Response adaptation in the barn owl's auditory space map.

Response adaptation is the change of the firing rate of neurons induced by a preceding stimulus. It can be found in many sensory systems and throughout the auditory pathway. We investigated response adaptation in the external nucleus of the inferior colliculus (ICX) of barn owls ( Tyto furcata), a nocturnal bird of prey and specialist in sound localization. Individual neurons in the ICX represent locations in auditory space by maximally responding to combinations of interaural time and level differences (ITD and ILD). Neuronal responses were recorded extracellularly under ketamine-diazepam anesthesia. Response adaptation was observed in three double stimulation paradigms. In two paradigms, the same binaural parameters for both stimuli were chosen. A variation of the level of the second stimulus yielded a level increase sufficient to compensate for adaptation around 5 dB. Introducing a silent interstimulus interval (ISI) resulted in recovery from adaptation. The time course of recovery was followed by varying the ISI, and full recovery was found after an ISI of 50 ms. In a third paradigm, the ITD of the second stimulus was varied to investigate the representation of ITD under adaptive conditions. We found that adaptation led to an increased precision and improved selectivity while the best ITD was stable. These changes of representation remained for longer ISIs than were needed to recover from response adaptation at the best ITD. Stimuli with non-best ITDs could also induce similar adaptive effects if the neurons responded to these ITDs. NEW & NOTEWORTHY We demonstrate and characterize response adaptation in neurons of the auditory space map in the barn owl's midbrain with acoustic double-stimulation paradigms. An increase of the second level by 5 dB compensated for the observed adaptive effect. Recovery from adaptation was faster than in upstream nuclei of the auditory pathway. Our results also show that response adaptation might improve precision and selectivity in the representation of interaural time difference.

The representation of sound localization cues in the barn owl's inferior colliculus.

The barn owl is a well-known model system for studying auditory processing and sound localization. This article reviews the morphological and functional organization, as well as the role of the underlying microcircuits, of the barn owl's inferior colliculus (IC). We focus on the processing of frequency and interaural time (ITD) and level differences (ILD). We first summarize the morphology of the sub-nuclei belonging to the IC and their differentiation by antero- and retrograde labeling and by staining with various antibodies. We then focus on the response properties of neurons in the three major sub-nuclei of IC [core of the central nucleus of the IC (ICCc), lateral shell of the central nucleus of the IC (ICCls), and the external nucleus of the IC (ICX)]. ICCc projects to ICCls, which in turn sends its information to ICX. The responses of neurons in ICCc are sensitive to changes in ITD but not to changes in ILD. The distribution of ITD sensitivity with frequency in ICCc can only partly be explained by optimal coding. We continue with the tuning properties of ICCls neurons, the first station in the midbrain where the ITD and ILD pathways merge after they have split at the level of the cochlear nucleus. The ICCc and ICCls share similar ITD and frequency tuning. By contrast, ICCls shows sigmoidal ILD tuning which is absent in ICCc. Both ICCc and ICCls project to the forebrain, and ICCls also projects to ICX, where space-specific neurons are found. Space-specific neurons exhibit side peak suppression in ITD tuning, bell-shaped ILD tuning, and are broadly tuned to frequency. These neurons respond only to restricted positions of auditory space and form a map of two-dimensional auditory space. Finally, we briefly review major IC features, including multiplication-like computations, correlates of echo suppression, plasticity, and adaptation.

Adaptation in the auditory midbrain of the barn owl (Tyto alba) induced by tonal double stimulation.

During hunting, the barn owl typically listens to several successive sounds as generated, for example, by rustling mice. As auditory cells exhibit adaptive coding, the earlier stimuli may influence the detection of the later stimuli. This situation was mimicked with two double-stimulus paradigms, and adaptation was investigated in neurons of the barn owl's central nucleus of the inferior colliculus. Each double-stimulus paradigm consisted of a first or reference stimulus and a second stimulus (probe). In one paradigm (second level tuning), the probe level was varied, whereas in the other paradigm (inter-stimulus interval tuning), the stimulus interval between the first and second stimulus was changed systematically. Neurons were stimulated with monaural pure tones at the best frequency, while the response was recorded extracellularly. The responses to the probe were significantly reduced when the reference stimulus and probe had the same level and the inter-stimulus interval was short. This indicated response adaptation, which could be compensated for by an increase of the probe level of 5-7 dB over the reference level, if the latter was in the lower half of the dynamic range of a neuron's rate-level function. Recovery from adaptation could be best fitted with a double exponential showing a fast (1.25 ms) and a slow (800 ms) component. These results suggest that neurons in the auditory system show dynamic coding properties to tonal double stimulation that might be relevant for faithful upstream signal propagation. Furthermore, the overall stimulus level of the masker also seems to affect the recovery capabilities of auditory neurons.

Estimated cochlear delays in low best-frequency neurons in the barn owl cannot explain coding of interaural time difference.

The functional role of the low-frequency range (<3 kHz) in barn owl hearing is not well understood. Here, it was tested whether cochlear delays could explain the representation of interaural time difference (ITD) in this frequency range. Recordings were obtained from neurons in the core of the central nucleus of the inferior colliculus. The response of these neurons varied with the ITD of the stimulus. The response peak shared by all neurons in a dorsoventral penetration was called the array-specific ITD and served as criterion for the representation of a given ITD in a neuron. Array-specific ITDs were widely distributed. Isolevel frequency response functions obtained with binaural, contralateral, and ispilateral stimulation exhibited a clear response peak and the accompanying frequency was called the best frequency. The data were tested with respect to predictions of a model, the stereausis model, assuming cochlear delays as source for the best ITD of a neuron. According to this model, different cochlear delays determined by mismatches between the ipsilateral and contralateral best frequencies are the source for the ITD in a binaural neuron. The mismatch should depend on the best frequency and the best ITD. The predictions of the stereausis model were not fulfilled in the low best-frequency neurons analyzed here. It is concluded that cochlear delays are not responsible for the representation of best ITD in the barn owl.

Target-approaching behavior of barn owls (Tyto alba): influence of sound frequency.

We studied the influence of frequency on sound localization in free-flying barn owls by quantifying aspects of their target-approaching behavior to a distant sound source during ongoing auditory stimulation. In the baseline condition with a stimulus covering most of the owls hearing range (1-10 kHz), all owls landed within a radius of 20 cm from the loudspeaker in more than 80% of the cases and localization along the azimuth was more accurate than localization in elevation. When the stimulus contained only high frequencies (>5 kHz) no changes in striking behavior were observed. But when only frequencies from 1 to 5 kHz were presented, localization accuracy and precision decreased. In a second step we tested whether a further border exists at 2.5 kHz as suggested by optimality models. When we compared striking behavior for a stimulus having energy from 2.5 to 5 kHz with a stimulus having energy between 1 and 2.5 kHz, no consistent differences in striking behavior were observed. It was further found that pre-takeoff latency was longer for the latter stimulus than for baseline and that center frequency was a better predictor for landing precision than stimulus bandwidth. These data fit well with what is known from head-turning studies and from neurophysiology.

Improvements of sound localization abilities by the facial ruff of the barn owl (Tyto alba) as demonstrated by virtual ruff removal.

BACKGROUND: When sound arrives at the eardrum it has already been filtered by the body, head, and outer ear. This process is mathematically described by the head-related transfer functions (HRTFs), which are characteristic for the spatial position of a sound source and for the individual ear. HRTFs in the barn owl (Tyto alba) are also shaped by the facial ruff, a specialization that alters interaural time differences (ITD), interaural intensity differences (ILD), and the frequency spectrum of the incoming sound to improve sound localization. Here we created novel stimuli to simulate the removal of the barn owl's ruff in a virtual acoustic environment, thus creating a situation similar to passive listening in other animals, and used these stimuli in behavioral tests. METHODOLOGY/PRINCIPAL FINDINGS: HRTFs were recorded from an owl before and after removal of the ruff feathers. Normal and ruff-removed conditions were created by filtering broadband noise with the HRTFs. Under normal virtual conditions, no differences in azimuthal head-turning behavior between individualized and non-individualized HRTFs were observed. The owls were able to respond differently to stimuli from the back than to stimuli from the front having the same ITD. By contrast, such a discrimination was not possible after the virtual removal of the ruff. Elevational head-turn angles were (slightly) smaller with non-individualized than with individualized HRTFs. The removal of the ruff resulted in a large decrease in elevational head-turning amplitudes. CONCLUSIONS/SIGNIFICANCE: The facial ruff a) improves azimuthal sound localization by increasing the ITD range and b) improves elevational sound localization in the frontal field by introducing a shift of iso-ILD lines out of the midsagittal plane, which causes ILDs to increase with increasing stimulus elevation. The changes at the behavioral level could be related to the changes in the binaural physical parameters that occurred after the virtual removal of the ruff. These data provide new insights into the function of external hearing structures and open up the possibility to apply the results on autonomous agents, creation of virtual auditory environments for humans, or in hearing aids.

In-flight corrections in free-flying barn owls (Tyto alba) during sound localization tasks.

Barn owls localize a stationary auditory target with high accuracy. They might also be able to hit a target that is intermittently moving while the owl is approaching. If so, there should be a critical delay before strike initiation, up to which the owl can adapt its flight path to a new stimulus position. In this study, this critical stimulus delay was determined in a three-dimensional free-flight paradigm. Barn owls localized a pulsed broadband noise while sitting on a perch in total darkness. This initial signal stopped with the owl's take-off and an in-flight stimulus (target sound), lasting 200 ms, was introduced at variable time delays (300-1200 ms) during the approximate flight time of 1300 ms. The owls responded to the in-flight signal with a corrective head and body turn. The percentage of trials in which correction turns occurred (40-80%) depended upon the individual bird, but was independent of the stimulus delay within a range of 800 ms after take-off. Correction turns strongly decreased at delays >or=800 ms. The landing precision of the owls, defined as their distance to the in-flight speaker, did not decrease with increasing stimulus delay, but decreased if the owl failed to perform a correction turn towards that speaker. Landing precision was higher for a short (50 cm) than for a large (100 cm) distance between the initial and the new target. Thus, the ability of barn owls to adapt their flight path to a new sound target depends on the in-flight stimulus delay, as well as on the distance between initial and novel targets.