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PubMed2006

Sound localization by barn owls in a simulated echoic environment.

We examined the accuracy and precision with which the barn owl (Tyto alba) turns its head toward sound sources under conditions that evoke the precedence effect (PE) in humans. Stimuli consisted of 25-ms noise bursts emitted from two sources, separated horizontally by 40 degrees, and temporally by 3-50 ms. At delays from 3 to 10 ms, head turns were always directed at the leading source, and were nearly as accurate and precise as turns toward single sources, indicating that the leading source dominates perception. This lead dominance is particularly remarkable, first, because on some trials, the lagging source was significantly higher in amplitude than the lead, arising from the directionality of the owl's ears, and second, because the temporal overlap of the two sounds can degrade the binaural cues with which the owl localizes sounds. With increasing delays, the influence of the lagging source became apparent as the head saccades became increasingly biased toward the lagging source. Furthermore, on some of the trials at delays > or = 20 ms, the owl turned its head, first, in the direction of one source, and then the other, suggesting that it was able to resolve two separately localizable sources. At all delays <50 ms, response latencies were longer for paired sources than for single sources. With the possible exception of response latency, these findings demonstrate that the owl exhibits precedence phenomena in sound localization similar to those in humans and cats, and provide a basis for comparison with neurophysiological data.

Acoustic Stimulation↗
PubMed2006

Adaptation in the auditory space map of the barn owl.

Auditory neurons in the owl's external nucleus of the inferior colliculus (ICX) integrate information across frequency channels to create a map of auditory space. This study describes a powerful, sound-driven adaptation of unit responsiveness in the ICX and explores the implications of this adaptation for sensory processing. Adaptation in the ICX was analyzed by presenting lightly anesthetized owls with sequential pairs of dichotic noise bursts. Adaptation occurred in response even to weak, threshold-level sounds and remained strong for more than 100 ms after stimulus offset. Stimulation by one range of sound frequencies caused adaptation that generalized across the entire broad range of frequencies to which these units responded. Identical stimuli were used to test adaptation in the lateral shell of the central nucleus of the inferior colliculus (ICCls), which provides input directly to the ICX. Compared with ICX adaptation, adaptation in the ICCls was substantially weaker, shorter lasting, and far more frequency specific, suggesting that part of the adaptation observed in the ICX was attributable to processes resident to the ICX. The sharp tuning of ICX neurons to space, along with their broad tuning to frequency, allows ICX adaptation to preserve a representation of stimulus location, regardless of the frequency content of the sound. The ICX is known to be a site of visually guided auditory map plasticity. ICX adaptation could play a role in this cross-modal plasticity by providing a short-term memory of the representation of auditory localization cues that could be compared with later-arriving, visual-spatial information from bimodal stimuli.

Acoustic Stimulation↗
PubMed2005

Microsecond precision of phase delay in the auditory system of the barn owl.

The auditory system encodes time with sub-millisecond accuracy. To shed new light on the basic mechanism underlying this precise temporal neuronal coding, we analyzed the neurophonic potential, a characteristic multiunit response, in the barn owl's nucleus laminaris. We report here that the relative time measure of phase delay is robust against changes in sound level, with a precision sharper than 20 micros. Absolute measures of delay, such as group delay or signal-front delay, had much greater temporal jitter, for example due to their strong dependence on sound level. Our findings support the hypothesis that phase delay underlies the sub-millisecond precision of the representation of interaural time difference needed for sound localization.

Acoustic Stimulation↗
PubMed2004

A neuronal correlate of the precedence effect is associated with spatial selectivity in the barn owl's auditory midbrain.

Sound localization in echoic conditions depends on a precedence effect (PE), in which the first arriving sound dominates the perceived location of later reflections. Previous studies have demonstrated neurophysiological correlates of the PE in several species, but the underlying mechanisms remain unknown. The present study documents responses of space-specific neurons in the barn owl's inferior colliculus (IC) to stimuli simulating direct sounds and reflections that overlap in time at the listener's ears. Responses to 100-ms noises with lead-lag delays from 1 to 100 ms were recorded from neurons in the space-mapped subdivisions of IC in anesthetized owls (N2O/isofluorane). Responses to a target located at a unit's best location were usually suppressed by a masker located outside the excitatory portion of the spatial receptive field. The least spatially selective units exhibited temporally symmetric effects, in that the amount of suppression was the same whether the masker led or lagged. Such effects mirror the alteration of localization cues caused by acoustic superposition of leading and lagging sounds. In more spatially selective units, the suppression was often temporally asymmetric, being more pronounced when the masker led. The masker often evoked small changes in spatial tuning that were not related to the magnitude of suppressive effects. The association of temporally asymmetric suppression with spatial selectivity suggests that this property emerges within IC, and not at earlier stages of auditory processing. Asymmetric suppression reduces the ability of highly spatially selective neurons to encode the location of lagging sounds, providing a possible basis for the PE.

Acoustic Stimulation↗
PubMed1999

Hearing impairment induces frequency-specific adjustments in auditory spatial tuning in the optic tectum of young owls.

Bimodal, auditory-visual neurons in the optic tectum of the barn owl are sharply tuned for sound source location. The auditory receptive fields (RFs) of these neurons are restricted in space primarily as a consequence of their tuning for interaural time differences and interaural level differences across broad ranges of frequencies. In this study, we examined the extent to which frequency-specific features of early auditory experience shape the auditory spatial tuning of these neurons. We manipulated auditory experience by implanting in one ear canal an acoustic filtering device that altered the timing and level of sound reaching the eardrum in a frequency-dependent fashion. We assessed the auditory spatial tuning at individual tectal sites in normal owls and in owls raised with the filtering device. At each site, we measured a family of auditory RFs using broadband sound and narrowband sounds with different center frequencies both with and without the device in place. In normal owls, the narrowband RFs for a given site all included a common region of space that corresponded with the broadband RF and aligned with the site's visual RF. Acute insertion of the filtering device in normal owls shifted the locations of the narrowband RFs away from the visual RF, the magnitude and direction of the shifts depending on the frequency of the stimulus. In contrast, in owls that were raised wearing the device, narrowband and broadband RFs were aligned with visual RFs so long as the device was in the ear but not after it was removed, indicating that auditory spatial tuning had been adaptively altered by experience with the device. The frequency tuning of tectal neurons in device-reared owls was also altered from normal. The results demonstrate that experience during development adaptively modifies the representation of auditory space in the barn owl's optic tectum in a frequency-dependent manner.

Adaptation, Physiological↗
PubMed2000

Horizontal-disparity tuning of neurons in the visual forebrain of the behaving barn owl.

Stereovision plays a major role in depth perception of animals having frontally-oriented eyes, most notably primates, cats, and owls. Neuronal mechanisms of disparity sensitivity have only been investigated in anesthetized owls so far. In the current study, responses of 160 visual Wulst neurons to static random-dot stereograms (RDS) were recorded via radiotelemetry in awake, fixating barn owls. The majority of neurons (76%) discharged significantly as a function of horizontal disparity in RDS. The distribution of preferred disparities mirrored the behaviorally relevant range of horizontal disparities that owls can exploit for depth vision. Most tuning profiles displayed periodic modulation and could well be fitted with a Gabor function as expected if disparity detectors were implemented according to the disparity energy model. Corresponding to this observation, a continuum of tuning profiles was observed rather than discrete categories. To assess a possible clustering of neurons with similar disparity-tuning properties, single units, and multi-unit activity recorded at individual recording sites were compared. Only a minority of neurons were clustered according to their disparity-tuning properties, suggesting that neurons in the visual Wulst are not organized into columns by preferred disparity. To assess whether variable vergence eye movements influenced tuning data, we correlated tuning peak positions on a trial-by-trial basis for units that were recorded simultaneously. The general lack of significant correlation between single-trial peak positions of simultaneously recorded units indicated that vergence, if at all, had only a minor influence on the data. Our study emphasizes the significance of visual Wulst neurons in analyzing stereoscopic depth information and introduces the barn owl as a second model system to study stereopsis in awake, behaving animals.

Action Potentials↗
PubMed2000

Representation of temporal features of complex sounds by the discharge patterns of neurons in the owl's inferior colliculus.

The spiking pattern evoked in cells of the owl's inferior colliculus by repeated presentation of the same broadband noise was found to be highly reproducible and synchronized with the temporal features of the noise stimulus. The pattern remained largely unchanged when the stimulus was presented from spatial loci that evoke similar average firing rates. To better understand this patterning, we computed the pre-event stimulus ensemble (PESE)-the average of the stimuli that preceded each spike. Computing the PESE by averaging the pressure waveforms produced a noisy, featureless trace, suggesting that the patterning was not synchronized to a particular waveform in the fine structure. By contrast, computing the PESE by averaging the stimulus envelope revealed an average envelope waveform, the "PESE envelope," typically having a peak preceded by a trough. Increasing the overall stimulus level produced PESE envelopes with higher amplitudes, suggesting a decrease in the jitter of the cell's response. The effect of carrier frequency on the PESE envelope was investigated by obtaining a cell's response to broadband noise and either estimating the PESE envelope for each spectral band or by computing a spectrogram of the stimulus prior to each spike. Either method yielded the cell's PESE spectrogram, a plot of the average amplitude of each carrier-frequency component at various pre-spike times. PESE spectrograms revealed surfaces with peaks and troughs at certain frequencies and pre-spike times. These features are collectively called the spectrotemporal receptive field (STRF). The shape of the STRF showed that in many cases, the carrier frequency can affect the PESE envelope. The modulation transfer function (MTF), which describes a cell's ability to respond to time-varying amplitudes, was estimated with sinusoidally amplitude-modulated (SAM) noises. Comparison of the PESE envelope with the MTF in the time and frequency domains showed that the two were closely matched, suggesting that a cell's response to SAM stimuli is largely predictable from its response to a noise-modulated carrier. The STRF is considered to be a model of the linear component of a system's response to dynamic stimuli. Using the STRF, we estimated the degree to which we could predict a cell's response to an arbitrary broadband noise by comparing the convolution of the STRF and the envelope of the noise with the cell's post-stimulus time histogram to the same noise. The STRF explained 18-46% of the variance of a cell's response to broadband noise.

Acoustic Stimulation↗
PubMed2001

Spatial attention modulates sound localization in barn owls.

Attentional influence on sound-localization behavior of barn owls was investigated in a cross-modal spatial cuing paradigm. After being cued to the most probable target side with a visual cuing stimulus, owls localized upcoming auditory target stimuli with a head turn toward the position of the sound source. In 80% of the trials, cuing stimuli pointed toward the side of the upcoming target stimulus (valid configuration), and in 20% they pointed toward the opposite side (invalid configuration). We found that owls initiated the head turns by a mean of 37.4 ms earlier in valid trials, i.e., mean response latencies of head turns were reduced by 16% after a valid cuing stimulus. Thus auditory stimuli appearing at the cued side were processed faster than stimuli appearing at the uncued side, indicating the influence of a spatial-selective attention mechanism. Turning angles were not different when owls turned their head toward a cued or an uncued location. Other types of attention influencing sound localization, e.g., a reduction of response latency as a function of the duration of cue-target delay, could not be observed. This study is the first attempt to investigate attentional influences on sound localization in an animal model.

Acoustic Stimulation↗
PubMed2001

Adaptive adjustment of connectivity in the inferior colliculus revealed by focal pharmacological inactivation.

In the midbrain sound localization pathway of the barn owl, a map of auditory space is synthesized in the external nucleus of the inferior colliculus (ICX) and transmitted to the optic tectum. Early auditory experience shapes these maps of auditory space in part by modifying the tuning of the constituent neurons for interaural time difference (ITD), a primary cue for sound-source azimuth. Here we show that these adaptive modifications in ITD tuning correspond to changes in the pattern of connectivity within the inferior colliculus. We raised owls with an acoustic filtering device in one ear that caused frequency-dependent changes in sound timing and level. As reported previously, device rearing shifted the representation of ITD in the ICX and tectum but not in the primary source of input to the ICX, the central nucleus of the inferior colliculus (ICC). We applied the local anesthetic lidocaine (QX-314) iontophoretically in the ICC to inactivate small populations of neurons that represented particular values of frequency and ITD. We measured the effect of this inactivation in the optic tecta of a normal owl and owls raised with the device. In the normal owl, inactivation at a critical site in the ICC eliminated responses in the tectum to the frequency-specific ITD value represented at the site of inactivation in the ICC. The location of this site was consistent with the known pattern of ICC-ICX-tectum connectivity. In the device-reared owls, adaptive changes in the representation of ITD in the tectum corresponded to dramatic and predictable changes in the locations of the critical sites of inactivation in the ICC. Given that the abnormal representation of ITD in the tectum depended on frequency and was likely conveyed directly from the ICX, these results suggest that experience causes large-scale, frequency-specific adjustments in the pattern of connectivity between the ICC and the ICX.

Adaptation, Physiological↗
PubMed2001

Early auditory experience induces frequency-specific, adaptive plasticity in the forebrain gaze fields of the barn owl.

Binaural acoustic cues such as interaural time and level differences (ITDs and ILDs) are used by many species to determine the locations of sound sources. The relationship between cue values and locations in space is frequency dependent and varies from individual to individual. In the current study, we tested the capacity of neurons in the forebrain localization pathway of the barn owl to adjust their tuning for binaural cues in a frequency-dependent manner in response to auditory experience. Auditory experience was altered by raising young owls with a passive acoustic filtering device that caused frequency-dependent changes in ITD and ILD. Extracellular recordings were made in normal and device-reared owls to characterize frequency-specific ITD and ILD tuning in the auditory archistriatum (AAr), an output structure of the forebrain localization pathway. In device-reared owls, individual sites in the AAr exhibited highly abnormal, frequency-dependent variations in ITD tuning, and across the population of sampled sites, there were frequency-dependent shifts in the representation of ITD. These changes were in a direction that compensated for the acoustic effects of the device on ITD and therefore tended to restore a normal representation of auditory space. Although ILD tuning was degraded relative to normal at many sites in the AAr of device-reared owls, the representation of frequency-specific ILDs across the population of sampled sites was shifted in the adaptive direction. These results demonstrate that early auditory experience shapes the representation of binaural cues in the forebrain localization pathway in an adaptive, frequency-dependent manner.

Acoustic Stimulation↗
PubMed1999

Visual fields in Short-toed Eagles, Circaetus gallicus (Accipitridae), and the function of binocularity in birds.

Visual fields were determined in alert restrained birds using an ophthalmoscopic reflex technique. The region of binocular overlap is relatively small: maximum width of 20 degrees occurs approximately 15 degrees below the horizontal, and the field extends vertically through 80 degrees with the bill tip placed close to the centre. Monocular field width in the horizontal plane is 139 degrees, and the field is asymmetric about the optic axis. The cyclopean field extends through 260 degrees, and the blind area above and behind the head reaches maximum width of 100 degrees close to the horizontal. At the frontal margins of the monocular field the retinal and optical fields do not coincide; the retinal field margin lies approximately 10 degrees inside the optical margin. This gives rise to an apparent binocular field that is twice the width of the functional binocular field. Interspecific comparisons show that the binocular field of Short-toed Eagles is similar in shape and size to those of bird species that differ markedly in phylogeny, ecology, foraging technique, and eye size. This suggests that these relatively narrow binocular fields are a convergent feature of birds whose foraging is guided by visual cues irrespective of whether items are taken directly in the bill or in the feet, as in eagles, and irrespective of the size and shape of the monocular and cyclopean visual fields. It is argued that binocular vision in birds results from the requirement for each monocular field to extend contralaterally to embody a portion of the optical flow field which is radially symmetrical about the direction of travel. This is in contrast to functional explanations of binocularity, such as those concerned with stereopsis, which present it as a means of extracting higher order information through the combination of two monocular images of the same portion of a scene.

Animals↗
PubMed1998

An additional bone in the sclera of the eyes of owls and the common potoo (Nictibius griseus) and its role in the contraction of the nictitating membrane.

Morphometric, anatomical and histological examinations were made in 10 species of owls of the families Tytonidae and Strigidae and compared with the eyes of other species of nocturnal birds including common potoo (Nictibiidae) and three species of nightjars (Caprimulgidae) and two diurnal species: the roadside hawk (Accipitridae) and the domestic duck (Anatidae). In owls and the common potoo the nictitating membrane is situated on the dorsal edge of the eye. In these birds, the scleral ring bears an additional, previously undescribed bone of various forms and dimensions (1.4-6.8 mm of length and 0.8-3.3 mm of width), located on the trajectory of the tendon of the pyramidal muscle which is attached to the nictitating membrane. This bone has a groove that encloses the tendon of the pyramidal muscle, preventing it from separating from the sclera during contraction, as well as diverting the trajectory of the tendon to impede it from projecting itself over the cornea. In the ferruginous pygmy owl, Nacunda nighthawk, Pauraque, scissor-tailed nightjar, roadside hawk and domestic duck the additional bone was not seen. Based on the morphofunctional characteristics of the bone, we suggest that this bone should be named the scleral sesamoid bone.

Animals↗
PubMed2001

Tonotopic and somatotopic representation in the nucleus basalis of the barn owl, Tyto alba.

We have investigated the somatosensory and auditory representations in the nucleus basalis of the barn owl. In pigeons and finches, the nucleus basalis contains a representation of the beak and an auditory area. In the barn owl, the nucleus basalis also contains a complete somatotopic map of the head and body (as in the budgerigar), with a tonotopically organized auditory area in close proximity to the representation of the facial ruff and the preaural area. Recordings within and around the nucleus basalis revealed predominantly (about 80%) contralateral responses to somatic stimulation. The somatotopic map was oriented with the head down and rostral. Penetrations revealed an over-representation of the feet in dorsal basalis, followed by the rest of the body and wings more ventrally. Towards more rostral positions in nucleus basalis, responses from the head and beak predominated ventrally. The auditory response area was encountered below the region that responded to stimulation of the facial ruff and preaural flap regions and above a region responsive to beak stimulation. Auditory responses were tonotopically organized, with low best frequencies dorsal. Some penetrations yielded predominantly monaural responses with a fairly broad dynamic range, similar to those recorded from the ventral nucleus of the lateral lemniscus (LLV) and the cochlear nucleus angularis, whereas other penetrations contained predominantly binaural responses sensitive to interaural time differences (ITD). The physiological responses could be predicted on the basis of auditory projections to the nucleus basalis. An injection of biotinylated dextran amine (BDA) in the auditory region of nucleus basalis retrogradely labeled cells in both the caudal and rostral parts of the intermediate lateral lemniscal nucleus (LLIc and LLIr), and a few cells in the anterior part of the dorsal lateral lemniscal nucleus (LLDa, previously known as nucleus ventralis lemnisci lateralis, pars anterior, or VLVa) and in the posterior part of the dorsal lateral lemniscal nucleus (LLDp, previously known as nucleus ventralis lemnisci lateralis, pars posterior, or VLVp). A large injection of cholera toxin B-chain (CTB) into the nucleus basalis also produced dense retrograde labeling of a previously unidentified nucleus on the lateral aspect of the rostral pons, that we here call nucleus pontis externus (PE). An injection of CTB into PE produced dense retrograde labeling of the contralateral dorsal column nuclei and anterograde labeling of the ipsilateral lateral and dorsolateral nucleus basalis. Together these results define major somatosensory and auditory projections to the owl telencephalon that bypass the thalamus.

Afferent Pathways↗
PubMed2003

Brain architecture and social complexity in modern and ancient birds.

Vertebrate brains vary tremendously in size, but differences in form are more subtle. To bring out functional contrasts that are independent of absolute size, we have normalized brain component sizes to whole brain volume. The set of such volume fractions is the cerebrotype of a species. Using this approach in mammals we previously identified specific associations between cerebrotype and behavioral specializations. Among primates, cerebrotypes are linked principally to enlargement of the cerebral cortex and are associated with increases in the complexity of social structure. Here we extend this analysis to include a second major vertebrate group, the birds. In birds the telencephalic volume fraction is strongly correlated with social complexity. This correlation accounts for almost half of the observed variation in telencephalic size, more than any other behavioral specialization examined, including the ability to learn song. A prominent exception to this pattern is owls, which are not social but still have very large forebrains. Interpolating the overall correlation for Archaeopteryx, an ancient bird, suggests that its social complexity was likely to have been on a par with modern domesticated chickens. Telencephalic volume fraction outperforms residuals-based measures of brain size at separating birds by social structure. Telencephalic volume fraction may be an anatomical substrate for social complexity, and perhaps cognitive ability, that can be generalized across a range of vertebrate brains, including dinosaurs.

Animals↗
PubMed2004

Bigger brains or bigger nuclei? Regulating the size of auditory structures in birds.

Increases in the size of the neuronal structures that mediate specific behaviors are believed to be related to enhanced computational performance. It is not clear, however, what developmental and evolutionary mechanisms mediate these changes, nor whether an increase in the size of a given neuronal population is a general mechanism to achieve enhanced computational ability. We addressed the issue of size by analyzing the variation in the relative number of cells of auditory structures in auditory specialists and generalists. We show that bird species with different auditory specializations exhibit variation in the relative size of their hindbrain auditory nuclei. In the barn owl, an auditory specialist, the hindbrain auditory nuclei involved in the computation of sound location show hyperplasia. This hyperplasia was also found in songbirds, but not in non-auditory specialists. The hyperplasia of auditory nuclei was also not seen in birds with large body weight suggesting that the total number of cells is selected for in auditory specialists. In barn owls, differences observed in the relative size of the auditory nuclei might be attributed to modifications in neurogenesis and cell death. Thus, hyperplasia of circuits used for auditory computation accompanies auditory specialization in different orders of birds.

Animals↗
PubMed1999

Evolution of time coding systems.

The auditory and electrosensory systems contain circuits that are specialized for the encoding and processing of microsecond time differences. Analysis of these circuits in two specialists, weakly electric fish and barn owls, has uncovered common design principles and illuminated some aspects of their evolution.

Algorithms↗
PubMed2003

Rodents in open space adjust their behavioral response to the different risk levels during barn-owl attack.

BACKGROUND: Previous studies have revealed that the response of prey species to predatory risk comprised either freezing (when the prey remained immobile), or fleeing (when it ran frantically in order to remove itself from the vicinity of the predator). Other studies, however, have suggested that the prey will adjust its behavior to risk level. The present study was designed to follow the attacks of a barn owl (Tyto alba) on common spiny mice (Acomys cahirinus) and social voles (Microtus socialis guntherei), in order to reveal the correspondence between the behavior of the owl, the risk level at each phase of the owl's attack, and the defensive behavior of the rodents. RESULTS: Spiny mice dramatically increased the traveled distance upon the appearance of the owl, and kept moving during its attack while taking long trajectories of locomotion. Defensive response in voles dichotomized: in some voles traveled distance dropped when the owl appeared, reaching zero during its attack. In other voles, traveled distance dramatically increased once the owl appeared and further increased under its attack. These defensive responses developed by gradual tuning of normal locomotor behavior in accordance with the level of risk. CONCLUSIONS: The phenotypic difference in defensive behavior between voles and spiny mice probably stems from their different habitats and motor capacities. Agility and running capacity, together with a relatively sheltered natural habitat, make fleeing the most appropriate response for spiny mice during owl attack. Clumsiness and relatively limited motor capacities, together with an open natural habitat, account for the dichotomy to freezing or fleeing in voles. Thus, the apparent species-specific anti-predator response in spiny mice and voles is based on species-specific normal locomotor behavior, which depends on the species-specific ecology and motor capacity, and behaviors like defensive attack or escape jump that are specific to life threat. The latter behaviors are brief, and irregularly inlaid in the ongoing locomotor behavior. Finally, our results show that in both voles and spiny mice there is a gradual transition from normal to defensive behavior in accordance with the increase in risk level.

Animals↗