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Development of the auditory brainstem of birds: comparison between barn owls and chickens.

Birds have proved to be extremely useful models for the study of hearing function. In particular, chickens and barn owls have been widely used by a number of researchers to study diverse aspects of auditory function. These studies have benefited from the advantages offered by each of these two species, including differences of auditory specialization. Direct comparisons between chickens and barn owls become complicated when the degree of auditory specialization and their modes of development are brought into consideration. In this article we review the available literature on the development of the auditory brainstem of chickens and barn owls in the context of such differences. In addition, we present a time line constructed on the basis of common stages of structural differentiation, rather than chronological time. We suggest that such a time line should be considered when discussing comparative data between these two species. Such an approach should facilitate the interpretation of similarities and differences observed in the developmental processes of the auditory system of chickens and barn owls.

Animals↗

Simulation of ILD sensitive neurons in the inferior colliculus of the barn owl.

The barn owl (Tyto alba) uses interaural level difference (ILD) as a cue for the localization of sound. The first site of binaural convergence in the pathway that processes ILD is the ventral lateral lemniscus pars posterior (VLVp). Neurons in VLVp receive excitatory input from the contralateral nucleus angularis, and inhibitory input from the contralateral VLVp. Within the lateral shell of the inferior colliculus are ILD sensitive neurons that show maximum spike rate at a specific ILD value, with response falling off sharply on each side. Adolphs has developed a model of such lateral shell neurons based on anatomic and physiological data. In his model, lateral shell neurons receive inhibitory input from VLVp on both sides, and this inhibition, applied against a constant excitatory input, produces the observed two-sided response curves. We simulated, in Matlab 4, Adolphs' model, and obtained supporting results. Our simulation suggests that VLVp provides a repository of simple ILD filters from which higher centers construct more complex filters, including the single-peaked curves observed by Adolphs. The VLVp filters are organized along the inhibitory gradient, with broad filters ventral, sharp filters dorsal.

Animals↗

General characteristics and suppression tuning properties of the distortion-product otoacoustic emission 2f1-f2 in the barn owl.

The distortion-product otoacoustic emission (DPOAE) 2f1-f2 was measured in the ear canal of the barn owl. DPOAE were elicited by primary tones in 11 frequency regions from 1 to 9 kHz. The highest DPOAE output levels and best thresholds were found for f1 frequencies of 4 to 7 kHz and additionally at the lowest f1 frequency investigated. In some cases, the DPOAE sound pressures were only 37 dB below the primary-tone levels (PTL). The optimal primary-tone frequency ratios ranged from 1.05 to 1.45 and varied strongly among the different frequency regions investigated. The largest optimal ratios were measured in the middle frequency range for f1. At lower and higher f1, the optimal ratios decreased. DPOAE levels could be suppressed in a frequency-selective way by adding a third tone. As in other non-mammals, the best suppressive frequencies were near f1, suggesting DPOAE generation near the frequency place of this primary tone. This is in contrast to what is known for mammalian species, where the DPOAE is thought to be generated near f2. To obtain 6 dB of suppression of the DPOAE level, suppressor-tone levels ranging from 13 dB below to 4 dB above the primary-tone level were necessary. The Q10dB-values of suppression tuning curves increased as a function of frequency up to a value of 15.8. This tendency resembled the increase in frequency selectivity of auditory nerve fibers in this species.

Acoustic Stimulation↗

Influence of contralateral acoustic stimulation on distortion-product and spontaneous otoacoustic emissions in the barn owl.

The avian auditory papilla provides an interesting object on which to study efferent influences, because whereas a significant population of hair cells in birds is not afferently innervated, all hair cells are efferently innervated (Fischer, 1992, 1994a, b). Previous studies in mammals using contralateral sound to stimulate the efferent system demonstrated a general suppressive effect on spontaneous and click-evoked, as well as on distortion-product otoacoustic emissions (DPOAE). As little is known about the effects of contralateral stimulation on hearing in birds, we studied the effect of such stimuli (broadband noise, pure tones) on the amplitude of the DPOAE 2f(1)-f(2) and on spontaneous otoacoustic emissions (SOAE) in the barn owl, Tyto alba. For the DPOAE measurements, fixed primary-tone pairs [f(1)=8.875 kHz (ratio=1.2), f(1)=8.353 kHz (ratio=1.15) and f(1)=7.889 kHz (ratio=1.1)] were presented and the DPOAE measured in the presence and absence of continuous contralateral stimulation. The DPOAE often declined in amplitude but in some cases we observed DPOAE enhancement. The changes in amplitude were as large as 9 dB. The influence of the contralateral noise changed over time, however, and the effects of contralateral tones were frequency-dependent. SOAE were suppressed in amplitude and shifted in frequency by contralateral broadband noise. Control measurements in animals after middle-ear muscle resection showed that these phenomena were not attributable to the acoustic middle-ear reflex. The finding of DPOAE enhancement is interesting, because a type of efferent fiber that suppressed its discharge rate during stimulation has been described in birds (Kaiser and Manley, 1994).

Acoustic Stimulation↗

Possible mechanisms for sensitivity to organophosphorus and carbamate insecticides in eastern screech-owls and American kestrels.

Effects of a single dietary exposure to fenthion and carbofuran on the survival, feeding behavior and brain ChE activity of eastern screech-owls, Otus asio and American kestrels, Falco sparverius, were evaluated. Birds were exposed to fenthion (23.6-189.0 ppm) or carbofuran (31.7-253.6 ppm) via meatballs. Carbofuran-exposed owls ate either < or = 10% or > or = 80% of the meatball whereas all kestrels ate < or = 10% of the meatball before exhibiting acute signs of toxicity. Fenthion-exposed owls and kestrels displayed a wide spectrum of meatball consumption (< 10-100%). Significant brain ChE inhibition was observed in dead and surviving kestrels exposed to fenthion and carbofuran and dead owls exposed to fenthion (P < 0.0001). Brain ChE activity of owls exposed to carbofuran that survived was not different from that of controls (P = 0.25). Data suggest: (1) slow feeding on a carbamate-contaminated item may provide limited protection from the toxicity of the chemical at certain rates of exposure; (2) the degree of ChE inhibition at neuromuscular junctions may be critical in determining the sensitivity of a species to a carbamate insecticide; (3) sensitivity may be a function of the ChE affinity for the carbamate inhibitor; and (4) the importance of neuromuscular junction ChE depression in determining the sensitivity of an animal may be species-specific.

Animals↗

The use of postmortem radiography as an aid in diagnosing, documenting, and understanding disease in animals.

Postmortem radiography can be a valuable supplement to traditional necropsy. This article provides examples where postmortem radiographs have been useful in diagnosing and documenting lesions in animals, and have helped demonstrate important principles of the pathology and the pathogenesis of lesions identified at necropsy. This article also discusses additional circumstances where the application of postmortem radiography might be worthwhile.

Animal Diseases↗

Effects of interaural decorrelation on neural and behavioral detection of spatial cues.

The detection of interaural time differences (ITDs) for sound localization critically depends on the similarity between the left and right ear signals (interaural correlation). We show that, like humans, owls can localize phantom sound sources well until the correlation declines to a very low value, below which their performance rapidly deteriorates. Decreasing interaural correlation also causes the response of the owl's tectal auditory neurons to decline nonlinearly, with a rapid drop followed by a more gradual reduction. A detection-theoretic analysis of the statistical properties of neuronal responses could account for the variance of behavioral responses as interaural correlation is decreased. Finally, cross-correlation analysis suggests that low interaural correlations cause misalignment of cross-correlation peaks across different frequencies, contributing heavily to the nonlinear decline in neural and ultimately behavioral performance.

Animals↗

Auditory processing in birds.

Over the past year, much progress has been achieved in the study of both the peripheral and the central auditory systems of birds. Significant advances have been made in the study of hair cells, including elucidation of the mechanisms of selectivity for sound frequency, functional differentiation, efferent innervation, and regeneration. Most of the studies of central auditory neurones have concerned the developmental and physiological correlates of vocal learning in songbirds and sound localisation in owls.

Acoustic Stimulation↗

Neural processing: the logic of multiplication in single neurons.

Theory indicates that neural networks can derive considerable computational power from a simple multiplication of their inputs, but the extent to which real neurons do this is unclear. A recent study of the auditory localization pathway of the barn owl has shed new light on this important question.

Animals↗

Study of sound localization by owls and its relevance to humans.

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

Animals↗

Heteroxenous coccidia increase the predation risk of parasitized rodents.

We have investigated the influence of heteroxenous coccidia (Apicomplexa: Eimeriorina) on the predation risk of intermediate hosts. Voles infected with Frenkelia spp. were found more frequently in buzzards' (Buteo buteo) prey than among snap-trapped rodents. To eliminate the possibility of traps selecting for uninfected rodents, a laboratory experiment was performed. Mice experimentally infected with Sarcocystis dispersa seemed to be more likely caught by the final host, the long-eared owl (Asio otus); this result was confirmed by a mathematical model. Field data confirmed the adaptive value of parasite-induced changes. The increase of predation is directed towards the specific final host only or is non-specific. In the populations studied the probability of predation of parasitized individuals by the specific predator was increased.

Animals↗

Encoding of both vertical and horizontal disparity in random-dot stereograms by Wulst neurons of awake barn owls.

In binocular vision, the lateral displacement of the eyes gives rise to both horizontal and vertical disparities between the images projected onto the left and right retinae. While it is well known that horizontal disparity is exploited by the binocular visual system of birds and mammals to enable depth perception, the role of vertical disparity is still largely unclear. In this study, neuronal activity in the visual forebrain (visual Wulst) of behaving barn owls to vertical disparity was investigated. Single-unit responses to global random-dot stereograms (RDS) were recorded with chronically implanted electrodes and transmitted via radiotelemetry. Nearly half of the cells investigated (44%, 16/36) varied the discharge as a function of vertical disparity. Like horizontal-disparity tuning profiles, vertical-disparity tuning curves typically exhibited periodic modulation with side peaks flanking a prominent main peak, and thus, could be fitted well with a Gabor function. This indicates that tuning to vertical disparity was not caused by disrupting horizontal-disparity tuning via vertical stimulus offset, but by classical disparity detectors whose orientation tuning was tilted. When tested with horizontal in addition to vertical disparity, almost all cells investigated (92%, 12/13) were tuned to both kinds of disparity. The emergence of disparity detectors sensitive in two dimensions (horizontal and vertical) is discussed within the framework of the disparity energy model.

Animals↗

Spatial variability and uncertainty in ecological risk assessment: a case study on the potential risk of cadmium for the little owl in a Dutch river flood plain.

This paper outlines a procedure that quantifies the impact of different sources of spatial variability and uncertainty on ecological risk estimates. The procedure is illustrated in a case study that estimates the risks of cadmium for a little owl (Athene noctua vidalli) living in a Dutch river flood plain along the river Rhine. A geographical information system (GIS) was used to quantify spatial variability in contaminant concentrations and habitats. It was combined with an exposure and effect model that uses Monte Carlo simulation to quantify parameter uncertainty. Spatial model uncertainty was assessed by the application of two different spatial interpolation methods (classification and kriging) and foraging ranges. The results of the case study show that parameter uncertainty is the main type of uncertainty influencing the risk estimate, and to a lesser extent spatial variability, while spatial model uncertainty was of minor importance. Compared to the deterministically calculated hazard index for the little owl (0.9), inclusion of spatial variability resulted in a median hazard index that can vary between 0.8 and 1.4. It is concluded that a single estimator for a whole flood plain may over- or underestimate risks for specific parts within the flood plain. Further research that expands the procedure presented in this paper is necessary to improve the incorporation of spatial factors in ecological risk assessment.

Animals↗

The rattling sound of rattlesnakes (Crotalus viridis) as a communicative resource for ground squirrels (Spermophilus beecheyi) and burrowing owls (Athene cunicularia).

Animal communication involves very dynamic processes that can generate new uses and functions for established communicative activities. In this article, the authors describe how an aposematic signal, the rattling sound of rattlesnakes (Crotalus viridis), has been exploited by 2 ecological associates of rattlesnakes: (a) California ground squirrels (Spermophilus beecheyi) use incidental acoustic cues in rattling sounds to assess the danger posed by the rattling snake, and (b) burrowing owls (Athene cunicularia) defend themselves against mammalian predators by mimicking the sound of rattling. The remarkable similarity between the burrowing owl's defensive hiss and the rattlesnake's rattling reflects both exaptation and adaptation. Such exploitation of the rattling sound has favored alternations in both the structure and the deployment of rattling by rattlesnakes.

Animal Communication↗

Neural bases of an auditory illusion and its elimination in owls.

Humans and owls localize sounds by detecting the arrival time disparity between the ears. Both species determine the interaural time difference by finding the delay necessary to match the leading signal with the lagging one. This method produces ambiguity with periodic signals, because the two signals can be matched by delaying either one or the other. As predicted, owls localized periodic signals in illusory directions, whereas they always perceived the real source when signal bandwidth exceeded a certain value. This bandwidth also enabled higher-order auditory neurons to discriminate between real and illusory sources.

Acoustic Stimulation↗

Perception and neuronal coding of subjective contours in the owl.

Robust form perception and underlying neuronal mechanisms require generalized representation of object boundaries, independent of how they are defined. One visual ability essential for form perception is reconstruction of contours absent from the retinal image. Here we show that barn owls perceive subjective contours defined by grating gaps and phase-shifted abutting gratings. Moreover, single-neuron recordings from visual forebrain (visual Wulst) of awake, behaving birds revealed a high proportion of neurons signaling such subjective contours, independent of local stimulus attributes. These data suggest that the visual Wulst is important in contour-based form perception and exhibits a functional complexity analogous to mammalian extrastriate cortex.

Animals↗