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Directional hearing by mechanical coupling in the parasitoid fly Ormia ochracea.

Sound localization is a basic processing task of the auditory system. The directional detection of an incident sound impinging on the ears relies on two acoustic cues: interaural amplitude and interaural time differences. In small animals, with short interaural distances both amplitude and time cues can become very small, challenging the directional sensitivity of the auditory system. The ears of a parasitoid fly Ormia ochracea, are unusual in that both acoustic sensors are separated by only 520 microns and are contained within an undivided air-filled chamber. This anatomy results in minuscule differences in interaural time cues (ca. 2 microseconds) and no measurable difference in interaural intensity cues generated from an incident sound wave. The tympana of both ears are anatomically coupled by a cuticular bridge. This bridge also mechanically couples the tympanana, providing a basis for directional sensitivity. Using laser vibrometry, it is shown that the mechanical response of the tympanal membranes has a pronounced directional sensitivity. Interaural time and intensity differences in the mechanical response of the ears are significantly larger than those available in the acoustic field. The tympanal membranes vibrate with amplitude differences of about 12 dB and time differences on the order of 50 microseconds to sounds at 90 degrees off the longitudinal body axis. The analysis of the deflection shapes of the tympanal vibrations shows that the interaural differences in the mechanical response are due to the dynamic properties of the tympanal system and reflect its intrinsic sensitivity to the direction of a sound source. Using probe microphones and extracellular recording techniques, we show that the primary auditory afferents encode sound direction with a time delay of about 300 microseconds. Our data point to a novel mechanism for directional hearing in O. ochracea based on intertympanal mechanical coupling, a process that amplifies small acoustic cues into interaural time and amplitude differences that can be reliably processed at the neural level. An intuitive description of the mechanism is proposed using a simple mechanical model in which the ears are coupled through a flexible lever.

Acoustics↗

Azimuthal processing in the posterior auditory thalamus of cats.

The responses to free-field acoustic stimuli of 157 units in the auditory thalamus of anesthetized cats were studied in relation to the localization of pure tone stimuli in the azimuthal plane. Units were classified as 'directional' if their firing rates at sound levels in excess of 20 dB above threshold varied by more than 50% as a function of azimuth. Sixty-five % of the units in the nucleus of the brachium of the inferior colliculus and 30% in the ventral division of the medial geniculate body were found to be directional, suggesting different processing channels for sound localization between colliculus and cortex.

Acoustic Stimulation↗

Lateralized auditory spatial perception and the contralaterality of cortical processing as studied with functional magnetic resonance imaging and magnetoencephalography.

Functional magnetic resonance imaging (fMRI) and magnetoencephalography (MEG) were used to study the relationships between lateralized auditory perception in humans and the contralaterality of processing in auditory cortex. Subjects listened to rapidly presented streams of short FM-sweep tone bursts to detect infrequent, slightly deviant tone bursts. The stimulus streams consisted of either monaural stimuli to one ear or the other or binaural stimuli with brief interaural onset delays. The onset delay gives the binaural sounds a lateralized auditory perception and is thought to be a key component of how our brains localize sounds in space. For the monaural stimuli, fMRI revealed a clear contralaterality in auditory cortex, with a contralaterality index (contralateral activity divided by the sum of contralateral and ipsilateral activity) of 67%. In contrast, the fMRI activations from the laterally perceived binaural stimuli indicated little or no contralaterality (index of 51%). The MEG recordings from the same subjects performing the same task converged qualitatively with the fMRI data, confirming a clear monaural contralaterality, with no contralaterality for the laterally perceived binaurals. However, the MEG monaural contralaterality (55%) was less than the fMRI and decreased across the several hundred millisecond poststimulus time period, going from 57% in the M50 latency range (20-70 ms) to 53% in the M200 range (170-250 ms). These data sets provide both quantification of the degree of contralaterality in the auditory pathways and insight into the locus and mechanism of the lateralized perception of spatially lateralized sounds.

Acoustic Stimulation↗

Altitude-dependent changes of directional hearing in mountaineers.

This study demonstrates apparent deterioration in the ability to localize sound associated with acute exposure to high altitude in ten subjects on three mountaineering expeditions. Furthermore, the auditory localization errors improved to sea level values after a period of acclimatization. Occurring at altitudes where overt neurological symptoms are not usually seen, impairment of sensory perception may explain the increase in accidental deaths associated with altitude exposure due to disorientation and misjudgment but before hypoxia is evident.

Acclimatization↗

Codes for sound-source location in nontonotopic auditory cortex.

We evaluated two hypothetical codes for sound-source location in the auditory cortex. The topographical code assumed that single neurons are selective for particular locations and that sound-source locations are coded by the cortical location of small populations of maximally activated neurons. The distributed code assumed that the responses of individual neurons can carry information about locations throughout 360 degrees of azimuth and that accurate sound localization derives from information that is distributed across large populations of such panoramic neurons. We recorded from single units in the anterior ectosylvian sulcus area (area AES) and in area A2 of alpha-chloralose-anesthetized cats. Results obtained in the two areas were essentially equivalent. Noise bursts were presented from loudspeakers spaced in 20 degrees intervals of azimuth throughout 360 degrees of the horizontal plane. Spike counts of the majority of units were modulated >50% by changes in sound-source azimuth. Nevertheless, sound-source locations that produced greater than half-maximal spike counts often spanned >180 degrees of azimuth. The spatial selectivity of units tended to broaden and, often, to shift in azimuth as sound pressure levels (SPLs) were increased to a moderate level. We sometimes saw systematic changes in spatial tuning along segments of electrode tracks as long as 1.5 mm but such progressions were not evident at higher sound levels. Moderate-level sounds presented anywhere in the contralateral hemifield produced greater than half-maximal activation of nearly all units. These results are not consistent with the hypothesis of a topographic code. We used an artificial-neural-network algorithm to recognize spike patterns and, thereby, infer the locations of sound sources. Network input consisted of spike density functions formed by averages of responses to eight stimulus repetitions. Information carried in the responses of single units permitted reasonable estimates of sound-source locations throughout 360 degrees of azimuth. The most accurate units exhibited median errors in localization of <25 degrees, meaning that the network output fell within 25 degrees of the correct location on half of the trials. Spike patterns tended to vary with stimulus SPL, but level-invariant features of patterns permitted estimates of locations of sound sources that varied through 20-dB ranges. Sound localization based on spike patterns that preserved details of spike timing consistently was more accurate than localization based on spike counts alone. These results support the hypothesis that sound-source locations are represented by a distributed code and that individual neurons are, in effect, panoramic localizers.

Action Potentials↗

Hearing in the ferret (Mustela putorius): effects of primary auditory cortical lesions on thresholds for pure tone detection.

1. Pure tone thresholds were determined for five adult male ferrets before and after bilateral ablation of primary auditory cortex. Complete audiograms ranging from 0.016 to 48 kHz were obtained for two animals. The remaining three animals were tested at five frequencies selected to assess hearing throughout the audible range (0.125, 0.5, 2.0, 8.0, and 32.0 kHz). 2. Shortly after surgery one animal had elevated thresholds across the entire frequency range with the most pronounced hearing loss above 12.0 kHz. Four other animals had no elevation of thresholds at low and midrange frequencies but suffered a hearing loss at very high frequencies (32 kHz). 3. Repeated testing over a period of several months revealed substantial recovery of sensitivity. There was complete recovery of sensitivity in the low- and middle-frequency range of the audiogram. Some hearing loss persisted at the extreme upper end of the audiogram (32 kHz), but in two cases there was evidence of recovery at this frequency as well. 4. Following determination of absolute thresholds all animals were assessed for their ability to localize sound in space. Minimum audible angles were obtained on midline as well as within both left and right hemifields, i.e., around 0, -60 and +60 degrees azimuth. All animals had severe and persistent deficits in their ability to localize brief sounds within the lateral fields, but were still capable of midline localization.

Animals↗

Localization of noise, use of binaural cues, and a description of the superior olivary complex in the smallest carnivore, the least weasel (Mustela nivalis).

Cats and dogs have relatively good sound-localization acuity, and the question arises as to whether this trait is a characteristic of all carnivores or whether it is due to the fact that they have large heads and correspondingly large binaural localization cues available to them. The localization acuity of the least weasel, the smallest extant carnivore, was found to be less accurate than larger carnivores but more accurate than other small mammals. This suggests that carnivores may be under strong selective pressure to localize accurately but that interaural distance may be a limiting factor. The least weasel is capable of using both binaural phase differences and intensity differences to localize, but has a relatively broad mid-frequency range for which neither cue is optimal. Finally, the superior olivary complex of the least weasel is well developed and resembles that of larger carnivores more than that of small rodents.

Animals↗

The auditory periphery of the ferret: postnatal development of acoustic properties.

The development of the acoustics of the auditory periphery of the ferret was examined by measuring the spectral transfer functions (STFs) and the directional characteristics of the outer ears of animals ranging in age from postnatal day 32 (P32) to P54. Using an impulse response technique the STFs were obtained from up to 250 locations throughout free space. The directional responses were calculated for frequencies between 1 kHz and 30 kHz. The low frequency roll-off of the STF decreased with increasing age from around 15 kHz at P32 to an adult value of around 8 kHz by P51. The directional responses of the outer ear of the immature ferrets differed significantly from adult animals in a fashion that was consistent with the smaller size of the auditory periphery. However, by P51 the responses were generally within the normal adult range. The implications of the relatively rapid development of the acoustics of the auditory periphery are discussed in terms of the development of mechanisms subserving sound localization.

Acoustic Stimulation↗

[Objective determinations of individual sound protectors (author's transl)].

A method for objective measurements of the sound attenuation provided by ear protectors is described, utilizing a head model which contains all normal human sound properties. The difficulties experienced in localizing sound sources when wearing ear protectors is explained by changing the characteristics of the individual frequency bands.

Ear Protective Devices↗

[Role of higher divisions of the auditory system in localizing a moving sound source].

Impairment of the ability to localize a moving acoustic image was studied in animal (dogs) following experimental ablation of the auditory cortical areas, and in patients following unilateral electro-shock seizures and focal injuries of the temporal cortex. Unilateral ablation of AI, AII and Ep areas in animals produces a disturbance in differentiation of parameters of a moving acoustic image, while a bilateral ablation results in disappearance of the ability to localize the image. After left-side electro-shock seizures in the patients, localization of movement of the acoustic image did not differ from the normal, while after right-side seizures, the trajectory of the image movement was sharply shortened and shifted to the right. In the case of a focal injury of the patient's left hemisphere, localization changes were of a diffuse nature (shortened trajectory of movement both on the right and left side). In the case of a right-side focus, the trajectory of the movement of the acoustic image on the side of the lesion did not differ from the normal, while on the opposite side it was sharply shortened and shifted towards the mid-line of the head. The conclusion has been made that there is a specialization in the human right hemisphere in achieving spatial hearing, while it is absent in animals.

Animals↗

Directionality of phase locking in auditory nerve fibers of the leopard frog Rana pipiens pipiens.

A dorsal approach to the eighth nerve and free-field stimulation were used to investigate the effect of sound direction and intensity on phase locking in auditory nerve fibers of the leopard frog Rana pipiens pipiens. Tuning curves of 75 auditory neurons were analyzed (Fig. 2). Amphibian papillar neurons, but not basilar papillar neurons, exhibit significant phase locking to short tone bursts at the characteristic frequency (CF), the degree of phase locking (vector strength) decreasing with the neuron's CF (Figs. 3, 4 and 10E). Vector strength increases with sound pressure level to saturate about 20 dB above threshold, while the preferred firing phase is only slightly affected (Figs. 5 and 6). In contrast, sound direction hardly affects vector strength (Figs. 7, 8, 9A and 10A and C), but has a strong influence on the preferred firing phase (Figs. 7, 8, 9B and C, 10B and D): With respect to anterior tone presentation there are phase lags for ipsilateral and phase leads for posterior and contralateral presentation. Phase differences between both ears show a sinusoidal or cardioid/ovoidal directional characteristic; maximum differences are found with antero-lateral tone presentation (Fig. 11). The directionality of phase locking decreases with the neuron's CF (Fig. 10F) and only slightly changes with sound pressure level (Fig. 12). Thus, phase locking of amphibian papilla neurons can potentially provide intensity-independent information for sound localization.

Acoustic Stimulation↗

Binaural tuning of auditory units in the forebrain archistriatal gaze fields of the barn owl: local organization but no space map.

We identified a region in the archistriatum of the barn owl forebrain that contains neurons sensitive to auditory stimuli. Nearly all of these neurons are tuned for binaural localization cues. The archistriatum is known to be the primary source of motor-related output from the avian forebrain and, in barn owls, contributes to the control of gaze, much like the frontal eye fields in monkeys. The auditory region is located in the medial portion of the archistriatum, at the level of the anterior commissure, and is within the region of the archistriatum from which head saccades can be elicited by electrical microstimulation (see preceding companion article, Knudsen et al., 1995). Free-field measurements revealed that auditory sites have large, spatial receptive fields. However, within these large receptive fields, responses are tuned sharply for sound source location. Dichotic measurements showed that auditory sites are tuned broadly for frequency and that the majority are tuned to particular values of interaural time differences and interaural level differences, the principal cues used by barn owls for sound localization. The tuning of sites to these binaural cues is essentially independent of sound level. The auditory properties of units in the medial archistriatum are similar to those of units in the optic tectum, a structure that also contributes to gaze control. Unlike the optic tectum, however, the auditory region of the archistriatum does not contain a single, continuous auditory map of space. Instead, it is organized into dorsoventral clusters of sites with similar binaural (spatial) tuning. The different representations of auditory space in closely related structures in the forebrain (archistriatum) and midbrain (optic tectum) probably reflect the fact that the forebrain contributes to a wide variety of sensorimotor tasks more complicated than gaze control.

Acoustic Stimulation↗

Auditory cortical responses to the interactive effects of interaural intensity disparities and frequency.

Under natural conditions, stimuli reaching the two ears contain multiple acoustic components. Rarely does a stimulus containing only one component (e.g. pure tone burst) exist outside the realm of the laboratory. For example, in sound localization the simultaneous presence of multiple cues (spectral content, level, phase, etc.) serves to increase the number of available cues and provide the listener with more information, thereby helping to reduce errors in locating the sound source. The present study was designed to explore the relationship between two acoustic parameters: stimulus frequency and interaural intensity disparities (IIDs). By varying both stimulus frequency and IIDs for each cell, we hoped to gain insight into how multiple cues are processed. To this end, we examined the responses of neurons in cat primary auditory cortex (AI) to determine if their sensitivity to IIDs changed as a function of stimulus frequency. IIDs ranging from +30 to -30 dB were presented at different frequencies (frequency was always the same in the two ears). We found that approximately half of the units examined exhibited responses to IIDs that varied as a function of stimulus frequency (i.e. displayed some form of IID x Freq dependency). The remaining units displayed IID responses that were not clearly related to stimulus frequency.

Acoustic Stimulation↗

[Directional hearing in relation to individual circadian biorhythm].

Acuity angle of the directional hearing was investigated in connection with the individual circadian rhythm. Two groups of 15 persons represented the morning and evening form of the circadian rhythm. Body temperature fixed the rhythm character. The evaluations of the angle acuity of the directional hearing were performed in the highest and the lowest point of body temperature as well as in the neutral point, which was determined in the morning group in the middle between the two extremes. The possibility of the sound localization in individual and linked with the body temperature circadian rhythm.

Acoustic Stimulation↗

An acoustic approach to diver navigation.

Three experiments were carried out to assess the capability of divers to localize acoustic signals underwater and to navigate by them. In the first experiment, divers attempted to determine the correct distance to several underwater transducers projecting acoustic stimuli on a horizontal plane. The second experiment consisted of two related studies where the diver/subjects attempted to discover which of many possible stimuli would produce the most robust perception of underwater "sound movement," or the Underwater Auditory Phi Phenomenon (UAPP). A third experiment consisted of navigational swims by divers; the acoustic stimuli utilized were based on those identified in prior experiments as the most preferred. The results demonstrated that divers are able to discriminate among signals emanating from acoustic sources at various distances underwater and to do so at levels well above chance. Second, divers judged 500-Hz square waves to be the signal which best facilitated an acceptable UAPP; thermal noise and 1-kHz square waves followed in that order. However, these differences were only slight and, in practice, divers maintained that the noise signal was the most useful. Third, it was found that divers apparently can effectively navigate by means of auditory signals alone--at least within certain limits. Finally, a significant decrease in the discrimination abilities of divers for frequencies above 6 kHz suggests that intensity cues may not be as robust as time-of-arrival information with respect to underwater sound localization.

Acoustic Stimulation↗

Directional dependence of interaural envelope delays.

Interaural envelope delays were measured in six human subjects as a function of the location of a movable sound source, bandpassed between 3 and 16 kHz. A total of 324 source locations were tested in horizontal and vertical increments of 10 degrees. A method is described for estimating the complex directional transfer function of the external ear, independent of the position of the recording microphone in the ear canal. To compute interaural envelope delays, directional transfer functions from the left and right ears were convolved with a critical-band filter, the envelopes were computed, and the envelopes were cross correlated. Interaural envelope delays, as well as interaural group delays, varied somewhat with the center frequency of the critical-band filter and with the vertical location of the sound source. Nevertheless, to a first approximation, envelope delays measured in the ear canals increased monotonically with increasing angle of incidence relative to the median plane, as they would for two microphones on the surface of a rigid sphere. The results are discussed in relation to the possible contribution of interaural envelope delays to sound localization behavior.

Attention↗

Neural derivation of sound source location: resolution of spatial ambiguities in binaural cues.

Cues for sound localization are inherently spatially ambiguous. Nevertheless, most neurons in the barn owl's optic tectum (superior colliculus) have receptive fields for broadband noise stimuli that are restricted to a single region of space. This study characterizes the spatial ambiguities associated with two important sets of localization cues, interaural level differences (ILDs) and interaural phase differences (IPDs), and describes how information is integrated within and across frequencies to resolve these ambiguities. The auditory receptive fields of neurons in the optic tectum were measured with free-field sounds presented from a movable loudspeaker. In contrast to the single regions typical for broadband receptive fields, receptive fields for tonal stimuli usually included additional discrete regions of space (accessory fields). Based on acoustic measurements of ILD and IPD cues made in the external ear canals, it was shown that accessory fields corresponded to locations from which sound sources produced ILD and IPD values that were approximately the same as those arising from the broadband receptive field. In addition, accessory fields had inhibitory surrounds, corresponding to locations from which sound sources produced substantially different combinations of ILD and IPD values. Where an accessory field for one frequency overlapped with the inhibitory surround of a second frequency, an excitatory response to the first frequency could be reduced or eliminated by addition of the second frequency. Because tonal receptive fields for different frequencies always overlapped in the region of the broadband receptive field but tended not to overlap elsewhere, this integration of excitation and inhibition can account for the restriction of broadband receptive fields to a single region of space.

Animals↗

Adaptive plasticity of the auditory space map in the optic tectum of adult and baby barn owls in response to external ear modification.

1. This study demonstrates the influence of experience on the establishment and maintenance of the auditory map of space in the optic tectum of the barn owl. Auditory experience was altered either by preventing the structures of the external ears (the facial ruff and preaural flaps) from appearing in baby barn owls (baby ruff-cut owls) or by removing these structures in adults (adult ruff-cut owls). These structures shape the binaural cues used for localizing sounds in both the horizontal and vertical dimensions. 2. The acoustic effects of removing the external ear structures were measured using probe tube microphones placed in the ear canals. In both baby and adult ruff-cut owls, the spatial pattern of binaural localization cues was dramatically different from normal: interaural level difference (ILD) changed with azimuth instead of with elevation, the rate of change of ILD across space was decreased relative to normal, and the rate of change of interaural time difference (ITD) across frontal space was increased relative to normal. 3. The neurophysiological representations of ITD and ILD in the optic tectum were measured before and > or = 3 mo after ruff removal in adults and beginning at 4.5 months of age in baby ruff-cut owls. Multiunit tuning to ITD and to ILD was measured using dichotic stimulation in ketamine-anesthetized owls. The tectal maps of ITD and ILD were reconstructed using visual receptive field location as a marker for recording site location in the optic tectum. 4. Adjustment of the tectal map of ITD to the altered spatial pattern of acoustic ITD was essentially complete in adults as well as in baby ruff-cut owls. This adjustment changed the magnification of ITD across the tectum, with resultant changes in ITD tuning at individual tectal sites of up to approximately 25 microseconds (approximately 5% of the physiological range) relative to normal values. 5. Adaptation of the tectal ILD map to the ruff-cut spatial pattern of acoustic ILD was substantial but clearly incomplete in both adult and baby ruff-cut owls. Although changes of up to approximately 15 dB (approximately 47% of the physiological range) relative to normal tuning were observed at certain tectal sites, the topography of the ILD map was always intermediate between normal and that predicted by the ruff-cut spatial pattern of acoustic ILD.(ABSTRACT TRUNCATED AT 400 WORDS)

Acoustic Stimulation↗