Barn Owl's Auditory Space Map Activity Matching Conditions for a Population Vector Readout to Drive Adaptive Sound-Localizing Behavior

Space-specific neurons in the owl''s midbrain form a neural map of auditory space, which supports sound-orienting behavior. Previous work proposed that a population vector (PV) readout of this map, implementing statistical inference, predicts the owl''s sound localization behavior. This model also predicts the frontal localization bias normally observed and how sound-localizing behavior changes when the signal-to-noise ratio varies, based on the spread of activity across the map. However, the actual distribution of population activity and whether this pattern is consistent with premises of the PV readout model on a trial-by-trial basis remains unknown. To answer these questions, we investigated whether the population response profile across the midbrain map in the optic tectum of the barn owl matches these predictions using in vivo multielectrode array recordings. We found that response profiles of recorded subpopulations are sufficient for estimating the stimulus interaural time difference using responses from single trials. Furthermore, this decoder matches the expected differences in trial-by-trial variability and frontal bias between stimulus conditions of low and high signal-to-noise ratio. These results support the hypothesis that a PV readout of the midbrain map can mediate statistical inference in sound-localizing behavior of barn owls.SIGNIFICANCE STATEMENT While the tuning of single neurons in the owl''s midbrain map of auditory space has been considered predictive of the highly specialized sound-localizing behavior of this species, response properties across the population remain largely unknown. For the first time, this study analyzed the spread of population responses across the map using multielectrode recordings and how it changes with signal-to-noise ratio. The observed responses support the hypothesis concerning the ability of a population vector readout to predict biases in orienting behaviors and mediate uncertainty-dependent behavioral commands. The results are of significance for understanding potential mechanisms for the implementation of optimal behavioral commands across species.     

Auditory processing of interaural timing information: new insights.

Differences in the time-of-arrival of sounds at the two ears, or interaural temporal disparities (ITDs), constitute one of the major binaural cues that underlie our ability to localize sounds in space. In addition, ITDs contribute to our ability to detect and to discriminate sounds, such as speech, in noisy environments. For low-frequency signals, ITDs are conveyed primarily by "cycle-by-cycle" disparities present in the fine-structure of the waveform. For high-frequency signals, ITDs are conveyed by disparities within the time-varying amplitude, or envelope, of the waveform. The results of laboratory studies conducted over the past few decades indicate that ITDs within the envelopes of high-frequency are less potent than those within the fine-structure of low-frequency stimuli. This is true for both measures of sensitivity to changes in ITD and for measures of the extent of the perceived lateral displacement of sounds containing ITDs. Colburn and Esquissaud (1976) hypothesized that it is differences in the specific aspects of the waveform that are coded neurally within each monaural (single ear) channel that account for the greater potency of ITDs at low frequencies rather than any differences in the more central binaural mechanisms that serve these different frequency regions. In this review, the results of new studies are reported that employed special high-frequency "transposed" stimuli that were designed to provide the high-frequency channels of the binaural processor with envelope-based information that mimics waveform-based information normally available only in low-frequency channels. The results demonstrate that these high-frequency transposed stimuli (1) yield sensitivity to ITDs that approaches, or is equivalent to, that obtained with "conventional" low-frequency stimuli and (2) yield large extents of laterality that are similar to those measured with conventional low-frequency stimuli. These findings suggest that by providing the high-frequency channels of the binaural processor with information that mimics that normally available only at low frequencies, the potency of ITDs in the two frequency regions can be made to be similar, if not identical. These outcomes provide strong support for Colburn and Esquissaud's (1976) hypothesis. The use of high-frequency transposed stimuli, in both behavioral and physiological investigations offers the promise of new and important insights into the nature of binaural processing.     

Neural correlates of binaural masking level difference in the inferior colliculus of the barn owl (Tyto alba)

Humans and animals are able to detect signals in noisy environments. Detection improves when the noise and the signal have different interaural phase relationships. The resulting improvement in detection threshold is called the binaural masking level difference. We investigated neural mechanisms underlying the release from masking in the inferior colliculus of barn owls in low‐frequency and high‐frequency neurons. A tone (signal) was presented either with the same interaural time difference as the noise (masker) or at a 180° phase shift as compared with the interaural time difference of the noise. The changes in firing rates induced by the addition of a signal of increasing level while masker level was kept constant was well predicted by the relative responses to the masker and signal alone. In many cases, the response at the highest signal levels was dominated by the response to the signal alone, in spite of a significant response to the masker at low signal levels, suggesting the presence of occlusion. Detection thresholds and binaural masking level differences were widely distributed. The amount of release from masking increased with increasing masker level. Narrowly tuned neurons in the central nucleus of the inferior colliculus had detection thresholds that were lower than or similar to those of broadly tuned neurons in the external nucleus of the inferior colliculus. Broadly tuned neurons exhibited higher masking level differences than narrowband neurons. These data suggest that detection has different spectral requirements from localization.     

Role of commissural projections in the representation of bilateral auditory space in the barn owl's inferior colliculus

The central nucleus of the barn owl's inferior colliculus (ICc) contains a representation of both the ipsilateral and contralateral auditory hemifields. The representation of ipsilateral space is found in the "core" of the ICc, a subdivision defined by the terminal field of nucleus laminaris, the avian analogue of the medial superior olivary nucleus. The representation of contralateral space is found in the lateral portion of the "shell" of the ICc. The shell surrounds the core and is defined by the terminal field of the nucleus angularis, one of the cochlear nuclei. The representation of ipsilateral space in the core of the ICc may be accounted for by the crossed projection from the nucleus laminaris because most of the nucleus laminaris is devoted to a representation of contralateral space. We present evidence to suggest that the representation of contralateral space is due to a commissural projection from the core of one side to the lateral shell of the opposite side. Injection of horseradish peroxidase (HRP) into the lateral portion of the ICc shell produced retrogradely labeled somata in the core of the opposite side. Injection of tritiated proline into the core produced anterograde label confined to the lateral shell, thus confirming the observations made with HRP. Thus, for example, the left ICc core, which contains predominantly a representation of the left hemifield, innervates the right lateral shell, endowing it with a representation of the left, or contralateral hemifield. The representation of contralateral space in the lateral shell is ultimately conveyed to the external nucleus of the inferior colliculus where it contributes the horizontal axis to a two-dimensional map of space.     

Kv1 currents mediate a gradient of principal neuron excitability across the tonotopic axis in the rat lateral superior olive

Principal neurons of the lateral superior olive (LSO) detect interaural intensity differences by integration of excitatory projections from ipsilateral bushy cells and inhibitory inputs from the medial nucleus of the trapezoid body. The intrinsic membrane currents active around firing threshold will form an important component of this binaural computation. Whole cell patch recording in an in vitro brain slice preparation was employed to study conductances regulating action potential (AP) firing in principal neurons. Current-clamp recordings from different neurons showed two types of firing pattern on depolarization, one group fired only a single initial AP and had low input resistance while the second group fired multiple APs and had a high input resistance. Under voltage-clamp, single-spiking neurons showed significantly higher levels of a dendrotoxin-sensitive, low threshold potassium current (ILT). Block of ILT by dendrotoxin-I allowed single-spiking cells to fire multiple APs and indicated that this current was mediated by Kv1 channels. Both neuronal types were morphologically similar and possessed similar amounts of the hyperpolarization-activated nonspecific cation conductance (Ih). However, single-spiking cells predominated in the lateral limb of the LSO (receiving low frequency sound inputs) while multiple-firing cells dominated the medial limb. This functional gradient was mirrored by a medio-lateral distribution of Kv1.1 immunolabelling. We conclude that Kv1 channels underlie the gradient of LSO principal neuron firing properties. The properties of single-spiking neurons would render them particularly suited to preserving timing information.     

Avian superior olivary nucleus provides divergent inhibitory input to parallel auditory pathways

The avian auditory brainstem displays parallel processing, a fundamental feature of vertebrate sensory systems. Nuclei specialized for temporal processing are largely separate from those processing other aspects of sound. One possible exception to this parallel organization is the inhibitory input provided by the superior olivary nucleus (SON) to nucleus angularis (NA), nucleus magnocellularis (NM), and nucleus laminaris (NL) and contralateral SON (SONc). We sought to determine whether single SON neurons project to multiple targets or separate neuronal populations project independently to individual target nuclei. We introduced two different fluorescent tracer molecules into pairs of target nuclei and quantified the extent to which retrogradely labeled SON neurons were double labeled. A large proportion of double-labeled SON somata were observed in all cases in which injections were made into any pair of ipsilateral targets (NA and NM, NA and NL, or NM and NL), suggesting that many individual SON neurons project to multiple targets. In contrast, when injections involved the SONc and any or all of the ipsilateral targets, double labeling was rare, suggesting that contralateral and ipsilateral targets are innervated by distinct populations of SON neurons arising largely from regionally segregated areas of SON. Therefore, at the earliest stages of auditory processing, there is interaction between pathways specialized to process temporal cues and those that process other acoustic features. We present a conceptual model that incorporates these results and suggest that SON circuitry, in part, functions to offset interaural intensity differences in interaural time difference processing.     

The Maturation of the Superior Collicular Map of Auditory Space in the Guinea Pig is Disrupted by Developmental Auditory Deprivation

Guinea pigs, reared from birth in an environment of omnidirectional white noise, fail to develop a map of auditory space in the deeper layers of the superior colliculus. Collicular responses from such noise-reared animals reveal large auditory spatial receptive fields. The representation of auditory space in the colliculus shows no topographic order. Exposing developing animals to the noise environment only for restricted time periods showed that animals reared normally up to 26 days after birth (DAB) and then placed in the noise chamber could not construct spatial maps, whereas animals reared normally to 30 DAB and then placed in the noise chamber until the terminal mapping experiment could construct topographically organized spatial maps with local receptive fields. Limiting the noise exposure to the period between 26 and 30 DAB was sufficient to prevent spatial map formation. The failure to form a map of auditory space did not reflect environmental damage to the cochlea or the functional organization of the primary auditory pathway. The response thresholds of cochlear microphonics and of auditory responses in both the inferior and superior colliculus were normal in noise-reared animals. Similarly normal were the tonotopic organization and frequency tuning characteristics of inferior collicular neurons. The rearing environment thus appears to exert a selective effect upon the maturation of the superior collicular map of auditory space. We attribute this effect to the masking, by the omnidirectional broad-band noise, of discrete localized auditory stimuli. Cues deriving from these latter stimuli would appear to be necessary for the elaboration of the map of auditory space. This auditory experience operates during a 4 day crucial developmental period from 26 to 30 DAB. This is the same developmental time window as that during which visual experience is required for the construction of the map.     

Acetylcholinesterase staining differentiates functionally distinct auditory pathways in the barn owl

The aim of this study was to examine how the functional specialization of the barn owl's auditory brainstem might correlate with histochemical compartmentalizaiton. The barn owl uses interaural intensity and time differences to encode, respectively, the vertical and azimuthal positions of sound sources in space. These two auditory cues are processed in parallel ascending pathways that separate from each other at the level of the cochlear nuclei. Sections through the auditory brainstem were stained for acetylcholinesterase (AChE) to examine whether nuclei that process different auditory cues stain differentially for this enzyme. Of the two cochlear nuclei, angularis showed more intense staining than nucleus magnocellularis. Nucleus angularis projects to all of the nuclei and subdivisions of nuclei that belong to the intensity processing pathway. Acetylcholinesterase stained all regions that contain terminal fields of nucleus angularis and thus provided discrimination between the time and intensity pathways. Moreover, staining patterns with acetylcholinesterase were complementary to those prevously reported with an anti-calbindin antibody, which stains terminal fields of nucleus laminaris, and thus stains all the nuclei and subdivisions of nuclei that belong to the time pathway. Some of the gross staining patterns observed with AChE were similar to those reported with antibodies to glutamate decarboxylase. However, AChE is a more convenient and definitive marker in discriminating between these pathways than is calbindin or glutamate decarboxylase. Acetylcholinesterase staining of the intensity pathway in the owl may be related to encoding of sound intensity by spike rate over large dynamic ranges. © 1993 Wiley-Liss, Inc.     

The Maturation of the Superior Collicular Map of Auditory Space in the Guinea Pig is Disrupted by Developmental Visual Deprivation

In the normal guinea pig a map of auditory space appears, in the deeper layers of the superior colliculus, at 32 days after birth (DAB). The animal is unable to construct this collicular map of auditory space in the absence of developmental visual experience. Auditory receptive fields of animals dark-reared from birth are typically large, occupying most of the contralateral hemifield. There is no topographic relationship between the collicular location of the recording electrode and the spatial position from which auditory stimuli elicit a maximal response. The fields of dark-reared animals resemble, in their tuning parameters, the spatially undifferentiated fields typical of young postnatal normal guinea pigs. To investigate the time-course during which visual experience is required for map emergence, animals received normal visual experience until either 18 or 26 DAB and were then dark-reared until the terminal mapping experiment. Maps developed in neither group. Animals provided with a normal visual environment until 30 DAB, and then placed in the dark did, however, construct topographically organized spatial maps with discrete spatial receptive fields. Maps also failed to emerge in animals receiving normal visual experience both before and after a 4-day period of visual deprivation between 26 and 30 DAB. We conclude that this 4-day period, or part of it, constitutes a 'crucial' period during which visual experience is required for the normal elaboration of the collicular map of auditory space.     

Auditory brainstem projections to the ferret superior colliculus: Anatomical contribution to the neural coding of sound azimuth

The mammalian superior colliculus (SC) contains a neural map of auditory space. It is not known whether this topographic representation emerges at the level of the SC or is relayed there from other auditory areas. We have used retrograde labelling techniques in ferrets to examine the sources and pattern of innervation from auditory brainstem nuclei. After multiple injections of wheat germ agglutinin conjugated to horseradish peroxidase (WGA-HRP) into the SC, the heaviest concentrations of labelled cells were found in the nucleus of the brachium (BIN) and external nucleus of the inferior colliculus, with much weaker labelling in the nucleus sagulum, dorsal, intermediate and ventral nuclei of the lateral lemniscus, paralemniscal regions, and periolivary nuclei. The projections were predominantly ipsilateral, although labelled cells were found on both sides of the brainstem. Single injections of WGA-HRP or discrete injections of red and green latex microspheres revealed that the caudal and lateral regions of the SC receive the heaviest projections, although the majority of the retrogradely labelled neurons in the contralateral BIN project to rostral SC. On the ipsilateral side, neurons in rostral and caudal regions of the BIN were labelled primarily by the tracer injected into rostral and caudal regions of the SC, respectively. However, no clear segregation was apparent in the BIN after injections into the medial and lateral regions or in any of the other nuclei after either injection paradigm. These data suggest that converging inputs from several auditory brainstem nuclei contribute to the construction of the auditory space map in the SC, although information about sound azimuth may be conveyed to this nucleus via a spatially ordered projection from the ipsilateral BIN. J. Comp. Neurol. 390:342–365, 1998. © 1998 Wiley-Liss, Inc.     

Receptive Fields of Neurons in the Owl's Auditory Brainstem Change Dynamically

Binaural neurons in the barn owl's auditory brainstem have spatial receptive fields. It is shown here that both the frequency tuning of these neurons and their tuning to interaural time difference (ITD), the prime cue for azimuthal sound localization, improves with time after stimulus onset, a process I shall term 'dynamic sharpening'. Thus, the receptive fields of these neurons also have a temporal dimension. Data were collected in four hierachically ordered nuclei concerned with the computation of ITD: the nucleus ventralis lemnisci lateralis, pars anterior (VLVa), and three subnuclei in the inferior colliculus. Dynamic sharpening in the frequency tuning curves is evident from a dynamic reduction of tuning width. When stimulated with a tone, the response of all neurons varies in a cyclic manner with ITD. The ITDs at the response peaks differ by one period of the stimulus tone. The responses with noise stimulation are similar to the responses with tonal stimulation in all but the hierarchically highest nucleus, the external nucleus of the inferior colliculus. In this nucleus are found neurons that, if stimulated with noise, respond maximally only to one ITD while the responses at the other peaks are suppressed. This sidepeak suppression is a dynamic process. Dynamic sharpening of ITD tuning is also evident from a dynamic reduction of the tuning width around each of the response peaks. The proportion of neurons showing dynamic sharpening of ITD tuning is the same in all collicular subnuclei, but is lower in VLVa. Therefore, a major component of dynamic sharpening of ITD tuning occurs at the first station of the inferior colliculus. Lateral inhibition is one of the mechanisms underlying dynamic sharpening. Part of the inhibition may be mediated by GABA (Fujita and Konishi, 1988). The function of dynamic sharpening of ITD tuning may be to increase the fine representation of auditory space in single neurons.     

Auditory Localization Behaviour in Visually Deprived Cats

The ability to localize sounds in azimuth was tested in five cats that had been binocularly deprived of vision from birth for several months and in three normal age-matched controls. Brief tone bursts were presented in an eight-choice apparatus along 360^° of the azimuthal plane at constant elevation. Using positive reinforcement techniques, the cats were trained to walk from the centre of the 3 m diameter circular enclosure to the hidden loudspeakers. The distribution of sound localization error from 55 trials per cat at each speaker position was measured, and its standard deviation was used to assess the precision of sound localization. All cats localized tones straight ahead of them most precisely; performance at lateral and rear positions was gradually less precise. When the sound localization ability of normal and binocularly deprived cats was compared across speakers, a significantly enhanced precision was found for binocularly deprived cats overall ( P < 0.002; two-way analysis of variance). An improvement was found at each individual speaker position, but it was greatest at lateral and rear positions. In two sets of control experiments normal cats were retested (i) in the dark with the aid of an infrared camera and (ii) after 3 months of binocular lid suture. Normal cats in the dark did not show any differences in their sound localization behaviour. Late-deprived cats showed a tendency for better performance, which fell short of statistical significance. Our results in visually deprived cats agree well with some reports on the sound localization ability of blind humans, but disagree with others. Our data provide support for a hypothesis of compensatory plasticity, in which sensory functions get sharpened with the loss of another modality. They seem to rule out the necessity for vision to play a role in the postnatal calibration of auditory space.     

Behavioural sensitivity to binaural spatial cues in ferrets: evidence for plasticity in the duplex theory of sound localization

For over a century, the duplex theory has guided our understanding of human sound localization in the horizontal plane. According to this theory, the auditory system uses interaural time differences (ITDs) and interaural level differences (ILDs) to localize low‐frequency and high‐frequency sounds, respectively. Whilst this theory successfully accounts for the localization of tones by humans, some species show very different behaviour. Ferrets are widely used for studying both clinical and fundamental aspects of spatial hearing, but it is not known whether the duplex theory applies to this species or, if so, to what extent the frequency range over which each binaural cue is used depends on acoustical or neurophysiological factors. To address these issues, we trained ferrets to lateralize tones presented over earphones and found that the frequency dependence of ITD and ILD sensitivity broadly paralleled that observed in humans. Compared with humans, however, the transition between ITD and ILD sensitivity was shifted toward higher frequencies. We found that the frequency dependence of ITD sensitivity in ferrets can partially be accounted for by acoustical factors, although neurophysiological mechanisms are also likely to be involved. Moreover, we show that binaural cue sensitivity can be shaped by experience, as training ferrets on a 1‐kHz ILD task resulted in significant improvements in thresholds that were specific to the trained cue and frequency. Our results provide new insights into the factors limiting the use of different sound localization cues and highlight the importance of sensory experience in shaping the underlying neural mechanisms.     

Synaptic depression improves coincidence detection in the nucleus laminaris in brainstem slices of the chick embryo

Neurons in the nucleus laminaris detect the coincidence of binaural signals, and are the first neurons to calculate the interaural time difference for the sound source localization in birds. In this paper, we have studied contributions of synaptic depression to the coincidence detection in the nucleus laminaris in a slice preparation of the chick embryo (E16-18), using the whole-cell patch recording technique. Under voltage clamp, EPSCs decreased progressively in their amplitude during the course of tetanic stimuli. This synaptic depression was primarily ascribed to the reduction of transmitter release from the presynaptic terminal, because the depression was decreased by reducing transmitter release with 2.5 microm Cd2+ but was not affected by reducing desensitization of postsynaptic AMPA receptors with 20 microm cyclothiazide. Under current clamp, trains of 10 stimuli of 100 Hz were applied bilaterally with changing the time intervals systematically between both sides. Response window, defined as the time interval corresponding to the half-maximum firing probability, was narrowed during the course of the stimulus train, and this occurred in parallel with a decrease in the EPSP amplitude. In addition, the reduction of the EPSP amplitude due to 2.5 microm Cd2+ or 2 microm CNQX improved the accuracy of coincidence detection. These results indicate that the synaptic depression may improve the coincidence detection in the chick laminaris neurons.     

Facilitation and Delay Sensitivity of Auditory Cortex Neurons in CF - FM Bats,Rhinolophus rouxi and Pteronotus p.parnellii

Responses of auditory neurons to complex stimuli were recorded in the dorsal belt region of the auditory cortex of two taxonomically unrelated bat species, Rhinolophus rouxi and Pteronotus parnellii parnellii, both showing Doppler shift compensation behaviour. As in P.p.parnellii (Suga et al., J. Neurophysiol., 49, 1573 - 1626, 1983), cortical neurons of R.rouxi show facilitated responses to pairs of pure tones or frequency modulations. Best frequencies for the two components lie near the first and second harmonic of the echolocation call but are in most cases not harmonically related. Neurons facilitated by pairs of pure tones show little dependence on the delay between the stimuli, whereas pairs of frequency modulations evoke best facilitated responses at distinct best delays between 1 and 10 ms. Facilitated neurons are found in distinct portions of the dorsal cortical belt region, with a segregation of facilitated neurons responding to pure tones and to frequency modulations. Non-facilitated neurons are found throughout the field. Neurons are topographically aligned with increasing best delays along a rostrocaudal axis. The best delays between 2 and 4 ms are largely overrepresented numerically, and occupy approximately 56% of the cortical area containing facilitated neurons. A functional interpretation of the large overrepresentation of best delays approximately 3 ms is proposed. Facilitated neurons are located almost entirely within layer V of the dorsal field.     

Efferent axons in the avian auditory nerve

The sensory hair cells of the inner ear receive both afferent and efferent innervation. The efferent supply to the auditory organ has evolved in birds and mammals into a separate complex system, with several types of neurons of largely unknown function. In this study, the efferent axons in four different species of birds (chicken, starling, barn owl and emu) were examined anatomically. Total numbers of efferents supplying the cochlear duct (auditory basilar papilla and the vestibular lagenar macula) were determined; separate estimates of the efferents to the lagenar macula only were also derived and subtracted. The numbers for auditory efferents thus varied between 120 (chicken) and 1068 (barn owl). Considering the much larger numbers of hair cells in the basilar papilla, each efferent is predicted to branch extensively. However, pronounced species-specific differences as well as regional differences along the tonotopic gradient of the basilar papilla were documented. Myelinated and unmyelinated axons were found, with mean diameters of about 1 microm and about 0.5 microm, respectively. This suggests two basic populations of efferents, however, they did not appear to be distinguished sharply. Evidence is presented that some efferents lose their myelination at the transition from central oligodendrocyte to peripheral Schwann cell myelin. Finally, a comparison of the four bird species evaluated suggests that the efferent population with smaller, unmyelinated axons is the phylogenetically more primitive one. A new population probably arose in parallel with the evolution and differentiation of the specialized hair-cell type it innervates, the short hair cell.     

Development of the representation of auditory space in the superior colliculus of the rat

The aims of the present study were, first, to determine the time of the emergence of the topographic map in the superior colliculus (SC) of the rat and, second, to examine the spatial changes in auditory neurons' receptive fields (RFs) throughout the developmental period. For these purposes, recording sessions were conducted on rats of different age groups (P15–18; P21–24; P27–29 and P60–80). Results show that SC auditory neurons' RFs go through multiple changes during early development before the establishment of the adult-like auditory topographic map (P27). These modifications include, first, the refining of directional RFs tuning between P18 and P27 and, second, a shift of sensitivity towards 90° in the contralateral hemispace after P15–18. In addition, data indicate that the neuronal response latencies are shorter in the adult group than in the P15–18 or P21–24 groups. Finally, a diminution in spontaneous firing rate was observed between the P15–18 group and the P60–80 group. The results of the present study revealed that the neural organization representing auditory space in the deep layers of the SC of the rat is not innate, but rather emerges at about P27–29. Moreover, they bring new evidence supporting a two-step process involved in the development of the representation of auditory space. Hence, the development of the auditory space representation follows a logical temporal maturation sequence whereby the RF organization must be completed before a stable topographic map can be formed.     

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.