An auditory fovea in the barn owl cochlea

The distribution of frequencies along the basilar papilla of the barn owl (Tyto alba) was studied by labelling small groups of primary auditory neurones of defined frequency response and tracing them to their peripheral innervation sites. The exact location of marked neurones was determined in cochlear wholemounts with the aid of a special surface preparation technique. The average basilar papilla length (in fixed, embedded specimens) was 10.74 mm.The resulting frequency map shows the basic vertebrate pattern with the lowest frequencies represented apically and increasingly higher frequencies mapped at progressively more basal locations. However, the length of basilar papilla devoted to different frequency ranges, i.e. the space per octave, varies dramatically in the barn owl. The lower frequencies (up to 2 kHz) show values between about 0.35 and 1 mm/octave, which are roughly equivalent to values reported for other birds. Above that, the space increases enormously, the highest octave (5–10 kHz) covering about 6 mm, or more than half of the length of the basilar papilla.Such an overrepresentation of a narrow, behaviourally very important frequency band is also seen in some bats, where it has been termed an acoustic or auditory fovea.Abbreviations CF characteristic frequency - HRP horseradish peroxidase - NA Nucleus angularis - NM Nucleus magnocellularis     

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

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

Restricted range of ocular accommodation in barn owls (Aves:Tytonidae)

Summary In an examination of the focusing abilities of 15 species of owls, the North American barn owl, Tyto alba pratincola (Bonaparte 1838), was an outstanding accommodator, having a range of accommodation exceeding 10 diopters (Murphy and Howland 1983). Using comparable methods, we examined the accommodation of 4 specimens of the Australian barn owl, Tyto alba delicatula (Gould 1837). We failed to elicit accommodation greater than two diopters, and most stimuli failed to evoke any discernable accommodation at all. Furthermore, examination of other Australian tytonid owls, the grass owl, T. longimembris, the sooty owl, T. tenebricosa, and both the mainland and Tasmanian subspecies of the masked owl, T. novaehollandiae novaehollandiae and T. novaehollandiae castanops, also failed to reveal anything but very moderate accommodative ranges. We conclude that the outstanding accommodative ability of the American barn owl is truly an exception to the modest accommodative abilities of the tytonid owls generally.     

Correlation between auditory sensitivity and vocalization in anabantoid fishes

Several anabantoid species produce broad-band sounds with high-pitched dominant frequencies (0.8–2.5 kHz), which contrast with generally low-frequency hearing abilities in (perciform) fishes. Utilizing a recently developed auditory brainstem response recording-technique, auditory sensitivities of the gouramis Trichopsis vittata, T. pumila, Colisa lalia, Macropodus opercularis and Trichogaster trichopterus were investigated and compared with the sound characteristics of the respective species. All five species exhibited enhanced sound-detecting abilities and perceived tone bursts up to 5 kHz, which qualifies this group as hearing specialists. All fishes possessed a high-frequency sensitivity maximum between 800 Hz and 1500 Hz. Lowest hearing thresholds were found in T. trichopterus (76 dB re 1 μPa at 800 Hz). Dominant frequencies of sounds correspond with the best hearing bandwidth in T. vittata (1–2 kHz) and C. lalia (0.8–1 kHz). In the smallest species, T. pumila, dominant frequencies of acoustic signals (1.5–2.5 kHz) do not match lowest thresholds, which were below 1.5 kHz. However, of all species studied, T. pumila had best hearing sensitivity at frequencies above 2 kHz. The association between high-pitched sounds and hearing may be caused by the suprabranchial air-breathing chamber, which, lying close to the hearing and sonic organs, enhances both sound perception and emission at its resonant frequency. Accepted: 26 November 1997     

Temporal modulation transfer functions in the barn owl (<Emphasis Type="Italic">Tyto alba</Emphasis>)

Barn owls (Tyto alba) have evolved several specializations in their auditory system to achieve the high sensory acuity required for prey capture, including superior processing of interaural time differences and phase coding in the auditory periphery. Here, we tested whether barn owls are capable of high temporal resolution that may be a prerequisite for the accuracy in binaural processing. Temporal resolution was measured psychoacoustically and demonstrated in temporal modulation transfer functions. Four barn owls were trained in an operant task with food reward to detect sinusoidal amplitude modulations within an 800-ms gated white-noise burst or 800-ms periods of modulation in continuous white noise (spectrum levels of -5 dB and 15 dB SPL). Within the range of tested amplitude modulation frequencies from 5 Hz to 1280 Hz, barn owls' detection thresholds were lowest at 10-20 Hz. This sensitivity corresponds to an intensity-difference limen of between 0.9 dB and 1.4 dB. For all conditions, temporal modulation transfer functions showed band-pass characteristics with a high-frequency cutoff in the range of 37 Hz to 92 Hz, corresponding to minimum integration times of 4.3 ms and 1.7 ms, respectively. In summary, these data indicate a temporal resolution in the owl's auditory system that is good, but not unusual, compared to other vertebrates.     

Pupillary dilation response as an indicator of auditory discrimination in the barn owl

The pupil of an awake, untrained, head-restrained barn owl was found to dilate in response to sounds with a latency of about 25 ms. The magnitude of the dilation scaled with signal-to-noise ratio. The dilation response habituated when a sound was repeated, but recovered when stimulus frequency or location was changed. The magnitude of the recovered response was related to the degree to which habituating and novel stimuli differed and was therefore exploited to measure frequency and spatial discrimination. Frequency discrimination was examined by habituating the response to a reference tone at 3 kHz or 6 kHz and determining the minimum change in frequency required to induce recovery. We observed frequency discrimination of 125 Hz at 3 kHz and 250 Hz at 6 kHz – values comparable to those reported by others using an operant task. Spatial discrimination was assessed by habituating the response to a stimulus from one location and determining the minimum horizontal speaker separation required for recovery. This yielded the first measure of the minimum audible angle in the barn owl: 3° for broadband noise and 4.5° for narrowband noise. The acoustically evoked pupillary dilation is thus a promising indicator of auditory discrimination requiring neither training nor aversive stimuli. Accepted: 28 February 2000     

Composition of the body mass overshoot in European barn owl nestlings (Tyto alba ): insurance against scarcity of energy or water?

European barn owl chicks (Tyto alba) show a body mass overshoot prior to fledging that has been predicted to serve as an energy reservoir during periods of stochastic food availability. However, the composition of the mass overshoot has heretofore not been directly examined in nestlings of this or any other species displaying a body mass overshoot during growth (e.g., raptors and seabirds). To experimentally determine whether the overshoot in body mass in juvenile European barn owls (Tyto alba) may act as an energy reservoir, we compared the body composition of owl chicks raised on an ad libitum diet to those fed a restricted diet designed to eliminate the overshoot. Chicks raised on the two diets were also compared for differences in maturation of diverse functions (e.g., locomotion) and tissues (e.g., skeletal development). Contrary to expectations, our results on body composition in juvenile barn owls indicate that the mass overshoot prior to fledging is primarily comprised of an increased water compartment. Thus, we suggest that the mass overshoot in owls (and possibly in other species) does not serve as an energy reservoir but, rather, may function as an insurance against dehydration when hot in-nest conditions force chicks to rely on evaporative cooling: temperatures in barn owl nests can reach up to 43 degrees C. We found no significant differences in maturation indexes between diet treatments at the time of fledging.     

Emmetropization and optical development of the eye of the barn owl (Tyto alba)

1. We have studied the development of the refractive state in young barn owls (Tyto alba pratincola). Strikingly, the eyes had severe refractive errors shortly after lid opening (which occurred around day 14 after hatching; average from 6 owls: 13.83 ± 1.47 days). Refractive errors vanished in the subsequent one or two weeks (Fig. 1, Fig. 2).
2. Refractive errors did not differ by more than 1 diopter (D) in both eyes of an individual (Fig. 2). Thus, non-visual control of eye growth was sufficient to produce non-random refractions. However, visual input was finally required to adjust the optical system to emmetropia.
3. Using in-vivo A-scan ultrasonography of ocular dimensions (Fig. 4A), photokeratometric measurements of corneal radius of curvature (Fig. 4B), and frozen sections of excised eyes (Fig. 3), we developed paraxial schematic eye models which described age-dependent changes in ocular parameters and were applicable through the ages from lid opening to fledging (Table 1). A schematic eye for the adult barn owl (European subspecies: Tyto alba alba) is also provided. Eye sizes in an adult owl of the American (Tyto alba pratincola) and the European subspecies (T. alba alba) were similar despite of different body weights (500 g and 350 g, respectively).
4. The schematic eyes were used to test which ocular parameters might have caused the recovery from refractive errors. However, none of the ocular dimensions measured underwent obvious changes in their growth curves as visual input became available. Apparently, coordinated growth of several ocular components produced emmetropia.
5. From the schematic eye model, the developmental changes in image brightness and image magnification were calculated (Fig. 5). In barn owl eyes, image size was not quite as extreme as in the tawny owl or the great horned owl. However, the image was larger and the f/number was lower than in diurnal birds of comparable weight (pigeon, chicken). The observation supports a conclusion that image size is maximised in owls to permit a higher degree of photoreceptor convergence for higher light sensitivity at dusk while spatial acuity remains comparable to diurnal birds with smaller eyes.

     

Analysis of spectral shape in the barn owl auditory system

In a behavioral experiment, we investigated how efficiently barn owls (Tyto alba) could detect changes in the spectral profile of multi-component auditory signals with stochastic envelope patterns. Signals consisted of one or five bands of noise (bandwidth 4, 16, or 64 Hz each; center frequencies 1.02, 1.43, 2.0, 2.8, 3.92 kHz). We determined increment thresholds for the 2 kHz component for three conditions: single-band condition (only the 2 kHz component), all five noise bands with the envelope fluctuations of the bands being either correlated or uncorrelated. Noise bandwidth had no significant effect on increment detection. Increment thresholds for the different conditions, however, differed significantly. Thresholds in correlated conditions were generally the lowest of all conditions, whereas, thresholds in uncorrelated conditions mostly resulted in the highest thresholds. This can be interpreted as evidence for comodulation masking release in barn owls. If the increment in the 2 kHz component is balanced by decrementing the four flanking bands in amplitude, increment detection thresholds are not affected. The data suggest that the barn owls used information from simultaneous spectral comparison across different frequency channels to detect spectral changes in multi-component noise signals rather than sequential comparison of overall stimulus levels.     

Direction of movements in Hungarian Barn Owls (Tyto alba): gene flow and barriers

Abstract. An analysis of dispersal directions of the barn owl showed that all individuals immigrating to Hungary came from W‐NW‐N. It was shown that immigrating owls breed in Hungary. There is no prevailing direction in emigration from Hungary. The time of fledging does not influence the direction of movement and there is no difference between sexes concerning dispersal direction. The percentages of emigrating owls is greater than that of immigrating ones. These percentages did not differ in relation to most of the analysed countries (Germany, Italy, Switzerland, Poland and countries of the former Yugoslavia and Czechoslovakia) but it differed in relation to Austria. The degree and direction of introgression into and from the transition zone and the recent distribution of the phenotypes are discussed based on the comparative analysis of published European data. These suggest that the subspecies Tyto alba alba and Tyto alba guttata disappear by introgression, to form a phenotypically very variable species.     

Isolation and characterization of 21 microsatellite markers in the barn owl (Tyto alba)

We report 21 new polymorphic microsatellite markers in the European barn owl (Tyto alba). The polymorphism of the reported markers was evaluated in a population situated in western Switzerland and in another from Tenerife, Canary Islands. The number of alleles per locus varies between two and 31, and expected heterozygosity per population ranges from 0.16 to 0.95. All loci are in Hardy-Weinberg equilibrium and no linkage disequilibrium was detected. Two loci exhibit a null allele in the Tenerife population.     

Characterization of beam patterns of bottlenose dolphin in the transverse plane

The characteristics of absolute auditory sensitivity of the bottlenose dolphin (Tursiops truncatus) in the transverse plane have been measured using short broadband stimuli simulating dolphin clicks (with energy maximum at frequencies 8, 16, 30, 50 and 100 kHz). Experiments were performed using the method of conditioned reflexes with food reinforcement. It is shown that, in the frequency range of 8–30 kHz, the absolute sensitivity of dolphin hearing in any ventral and lateral directions of the transverse plane is only 2–8 dB worse than in the rostral direction. Moreover, it is 25–30 dB better than at 50–100 kHz. At 8–30 kHz, pronounced dorsoventral asymmetry has been observed. In this frequency range, it reaches 15–18 dB whereas at 50–100 kHz this asymmetry decreases to 2–3 dB. In the dorsal direction, the auditory sensitivity is 18 dB worse than in the rostral one at ∼8 kHz, and the difference rises smoothly to 33 dB at ∼100 kHz. At 50–100 kHz, the acoustical thresholds in the transverse plane relative to those for the with rostral direction get worse almost uniformly in all directions by 25–33 dB. As a result, in the transverse plane the beam patterns are nearly circular, unlike those at 8–30 kHz. The results are discussed in terms of the model of sound perception through the left and right mental foramens. The biological relevance of such asymmetry is emphasized.     

Psychophysical and neurophysiological hearing thresholds in the bat <Emphasis Type="Italic">Phyllostomus </Emphasis><Emphasis Type="Italic">discolor</Emphasis>

Absolute hearing thresholds in the spear-nosed bat Phyllostomus discolor have been determined both with psychophysical and neurophysiological methods. Neurophysiological data have been obtained from two different structures of the ascending auditory pathway, the inferior colliculus and the auditory cortex. Minimum auditory thresholds of neurons are very similar in both structures. Lowest absolute thresholds of 0 dB SPL are reached at frequencies from about 35 to 55 kHz in both cases. Overall behavioural sensitivity is roughly 20 dB better than neural sensitivity. The behavioural audiogram shows a first threshold dip around 23 kHz but threshold was lowest at 80 kHz (−10 dB SPL). This high sensitivity at 80 kHz is not reflected in the neural data. The data suggest that P. discolor has considerably better absolute auditory thresholds than estimated previously. The psychophysical and neurophysiological data are compared to other phyllostomid bats and differences are discussed. S. Hoffmann, L. Baier, F. Borina contributed equally to this work.     

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     

Directional hearing in the barn owl (Tyto alba)

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

Sensory basis for sound intensity discrimination in the bushcricket Requena verticalis (Tettigoniidae, Orthoptera)

The ability of the female bushcricket, Requena verticalis, to discriminate between two conspecific sound signals that differed in sound pressure level (SPL) was tested in a two-choice paradigm. Significant discrimination was achieved with a 2-dB difference. The property of each pair of receptors to establish binaural discharge differences was investigated in electrophysiological experiments. The threshold to the conspecific signal varies for each fibre from about 40 to 90 dB SPL, allowing for a range fractionation of the hearing organ. Each pair of receptors establishes significant binaural discharge differences only within a restricted intensity range about 10 dB above threshold. Based on a model of the intensity response function of a receptor the total discharge of the 22 receptors in both ears was calculated with monaural and binaural stimulation. The profile of receptors exhibiting significant discharge differences changes with increasing SPL, from the most sensitive fibres with a characteristic frequency between 12 kHz and 35 kHz at low SPLs to the least sensitive fibres at very low and high characteristic frequencies at medium to high SPLs. The discharge difference with an intensity difference of 2 dB is rather small (4% of the total receptor activity) and limited only to a few pairs of receptors. Accepted: 8 November 1997     

Microsatellite markers characterized in the barn owl (Tyto alba) and of high utility in other owls (Strigiformes: AVES)

We have identified 15 polymorphic microsatellite loci for the barn owl (Tyto alba), five from testing published owl loci and 10 from testing non‐owl loci, including loci known to be of high utility in passerines and shorebirds. All 15 loci were sequenced in barn owl, and new primer sets were designed for eight loci. The 15 polymorphic loci displayed two to 26 alleles in 56–58 barn owls. When tested in 10 other owl species (n = 1–6 individuals), between four and nine loci were polymorphic per species. These loci are suitable for studies of population structure and parentage in owls.     

Binocular responses of neurons in the barn owl's visual Wulst

Binocular responses have been recorded extra-cellularly at 58 sites in the barn owl's (Tyto alba) visual Wulst. Neurons showed disparity tuning to stimulation with moving bars, moving sinewave gratings and a moving visual-noise stimulus. Responses to sinewave gratings as a function of disparity were cyclic, with the period of a cycle of the response being correlated to one cycle of the stimulus. Cyclic responses were also found when bars or noise were used as a stimulus, but, especially in response to visual noise, one response peak, the main peak, was different from the other peaks, the sidepeaks: usually, the main peak was either higher or narrower or both higher and narrower than the sidepeaks. When the responses to different spatial frequencies were compared, response maxima coincided at the main peak, but not at the other peaks. In analogy to auditory physiology the disparity at which the frequency-independent peak occurs is termed characteristic disparity. Spatial-frequency tuning revealed broad tuning, ranging from 1 to more than 3 octaves at 50% of the maximal response. Disparity tuning was broad at the onset of the response and sharpened later. The data are discussed within the framework of a model for the neural representation of visual disparity that was derived from a model proposed earlier for the representation of interaural time difference, the main cue for encoding sound-source azimuths in the barn owl.Abbreviations ITD interaural time difference - CD characteristic delay - RF receptive field