Owl Auditory System Research Articles

Cue Reliability Represented in the Shape of Tuning Curves in the Owl's Sound Localization System.

In natural environments, sensory cues are often corrupted by noise and are therefore unreliable. To make the best decisions, the brain must estimate the degree to which a cue can be trusted. The behaviorally relevant neural correlates of cue reliability are debated. In this study, we used the barn owl's sound localization system to address this question. We demonstrated that the mechanisms that account for spatial selectivity also explained how neural responses changed with degraded signals. This allowed for the neurons' selectivity to capture cue reliability, influencing the population readout commanding the owl's sound-orienting behavior.

Bifurcation of learning and structure formation in neuronal maps

Most learning processes in neuronal networks happen on a much longer time scale than that of the underlying neuronal dynamics. It is therefore useful to analyze slowly varying macroscopic order parameters to explore a network's learning ability. We study the synaptic learning process giving rise to map formation in the laminar nucleus of the barn owl's auditory system. Using equation-free methods, we perform a bifurcation analysis of spatio-temporal structure formation in the associated synaptic-weight matrix. This enables us to analyze learning as a bifurcation process and follow the unstable states as well. A simple time translation of the learning window function shifts the bifurcation point of structure formation and goes along with traveling waves in the map, without changing the animal's sound localization performance.

Modeling the Nucleus Laminaris of the Barn Owl: Achieving 20 ps Resolution on a 85-MHz-Clocked Digital Device

The nucleus laminaris of the barn owl auditory system is quite impressive, since its underlying time estimation is much better than the processing speed of the involved neurons. Since precise localization is also very important in many technical applications, this paper explores to what extent the main principles of the nucleus laminaris can be implemented in digital hardware. The first prototypical implementation yields a time resolution of about 20 ps, even though the chosen standard, low-cost device is clocked at only 85 MHz, which leads to an internal duty cycle of approximately 12 ns. In addition, this paper also explores the utility of an advanced sampling scheme, known as unfolding-in-time. It turns out that with this sampling method, the prototype can easily process input signals of up to 300 MHz, which is almost four times higher than the sampling rate.

Relative Size of Auditory Pathways in Symmetrically and Asymmetrically Eared Owls

Owls are highly efficient predators with a specialized auditory system designed to aid in the localization of prey. One of the most unique anatomical features of the owl auditory system is the evolution of vertically asymmetrical ears in some species, which improves their ability to localize the elevational component of a sound stimulus. In the asymmetrically eared barn owl, interaural time differences (ITD) are used to localize sounds in azimuth, whereas interaural level differences (ILD) are used to localize sounds in elevation. These two features are processed independently in two separate neural pathways that converge in the external nucleus of the inferior colliculus to form an auditory map of space. Here, we present a comparison of the relative volume of 11 auditory nuclei in both the ITD and the ILD pathways of 8 species of symmetrically and asymmetrically eared owls in order to investigate evolutionary changes in the auditory pathways in relation to ear asymmetry. Overall, our results indicate that asymmetrically eared owls have much larger auditory nuclei than owls with symmetrical ears. In asymmetrically eared owls we found that both the ITD and ILD pathways are equally enlarged, and other auditory nuclei, not directly involved in binaural comparisons, are also enlarged. We suggest that the hypertrophy of auditory nuclei in asymmetrically eared owls likely reflects both an improved ability to precisely locate sounds in space and an expansion of the hearing range. Additionally, our results suggest that the hypertrophy of nuclei that compute space may have preceded that of the expansion of the hearing range and evolutionary changes in the size of the auditory system occurred independently of phylogeny.

Learning Drives Differential Clustering of Axodendritic Contacts in the Barn Owl Auditory System

Computational models predict that experience-driven clustering of coactive synapses is a mechanism for information storage. This prediction has remained untested, because it is difficult to approach through time-lapse analysis. Here, we exploit a unique feature of the barn owl auditory localization pathway that permits retrospective analysis of prelearned and postlearned circuitry: owls reared wearing prismatic spectacles develop an adaptive microcircuit that coexists with the native one but can be analyzed independently based on topographic location. To visualize the clustering of axodendritic contacts (potential synapses) within these zones, coactive axons were labeled by focal injection of fluorescent tracer and their target dendrites labeled with an antibody directed against CaMKII (calcium/calmodulin-dependent protein kinase type II, alpha subunit). Using high-resolution confocal imaging, we measured the distance from each contact to its nearest neighbor on the same branch of dendrite. We found that the distribution of intercontact distances for the adaptive zone was shifted dramatically toward smaller values compared with distributions for either the maladaptive zone of the same animals or the adaptive zone of normal juveniles, which indicates that a dynamic clustering of contacts had occurred. Moreover, clustering in the normal zone was greater in normal juveniles than in prism-adapted owls, indicative of declustering. These data demonstrate that clustering is bidirectionally adjustable and tuned by behaviorally relevant experience. The microanatomical configurations in all zones of both experimental groups matched the functional circuit strengths that were assessed by in vivo electrophysiological mapping. Thus, the observed changes in clustering are appropriately positioned to contribute to the adaptive strengthening and weakening of auditory-driven responses.

Passive Soma Facilitates Submillisecond Coincidence Detection in the Owl's Auditory System

Neurons of the avian nucleus laminaris (NL) compute the interaural time difference (ITD) by detecting coincident arrivals of binaural signals with submillisecond accuracy. The cellular mechanisms for this temporal precision have long been studied theoretically and experimentally. The myelinated axon initial segment in the owl's NL neuron and small somatic spikes observed in auditory coincidence detector neurons of various animals suggest that spikes in the NL neuron are generated at the first node of Ranvier and that the soma passively receives back-propagating spikes. To investigate the significance of the "passive soma" structure, we constructed a two-compartment NL neuron model, consisting of a cell body and a first node, and systematically changed the excitability of each compartment. Here, we show that a neuron with a less active soma achieves higher ITD sensitivity and higher noise tolerance with lower energy costs. We also investigate the biophysical mechanism of the computational advantage of the "passive soma" structure by performing sub- and suprathreshold analyses. Setting a spike initiation site with high sodium conductance, not in the large soma but in the small node, serves to amplify high-frequency input signals and to reduce the impact and the energy cost of spike generation. Our results indicate that the owl's NL neuron uses a "passive soma" design for computational and metabolic reasons.

Analysis of spectral shape in the barn owl auditory system

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

Binaural processing in the synthesis of auditory spatial receptive fields.

The owl's auditory system computes interaural time (ITD) and interaural level (ILD) differences to create a two-dimensional map of auditory space. Space-specific neurons are selective for combinations of ITD and ILD, which define, respectively, the horizontal and vertical dimensions of their receptive fields. ITD curves for postsynaptic potentials indicate that ICx neurons integrate the results of binaural cross correlation in different frequency bands. However, the difference between the main and side peaks is slight. ICx neurons further enhance this difference in the process of converting membrane potentials to impulse rates. Comparison of subthreshold postsynaptic potentials (PSPs) and spike output for the same neurons showed that receptive fields measured in PSPs were much larger than those measured in spikes in both ITD and ILD dimensions. A multiplication of separate postsynaptic potentials tuned to ITD and ILD can account for the combination sensitivity of these neurons to ITD-ILD pairs.

Temporal modulation transfer functions in the barn owl (Tyto alba).

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

Auditory spatial receptive fields created by multiplication.

Examples of multiplication by neurons or neural circuits are scarce, although many computational models use this basic operation. The owl's auditory system computes interaural time (ITD) and level (ILD) differences to create a two-dimensional map of auditory space. Space-specific neurons are selective for combinations of ITD and ILD, which define, respectively, the horizontal and vertical dimensions of their receptive fields. A multiplication of separate postsynaptic potentials tuned to ITD and ILD, rather than an addition, can account for the subthreshold responses of these neurons to ITD-ILD pairs. Other nonlinear processes improve the spatial tuning of the spike output and reduce the fit to the multiplicative model.

A Candidate Pathway for a Visual Instructional Signal to the Barn Owl's Auditory System

Many organisms use multimodal maps to generate coherent neuronal representations that allow adequate responses to stimuli that excite several sensory modalities. During ontogeny of these maps, one modality typically acts as the dominant system the other modalities are aligned to. A well studied model for the alignment of sensory maps is the calibration of the auditory space map by the visual system in the optic tectum of the barn owl. However, a projection from the optic tectum to the site of plasticity in the auditory pathway that could deliver an instructive signal has not been found so far. We have analyzed the development of the connectivity between the bimodal (visual and auditory) map of space in the barn owl's optic tectum and the auditory space map in the inferior colliculus with tracing methods and intracellular fills. Neurons in the tectal stratum griseum centrale were found to be suited to deliver an alignment signal from the visual midbrain to the auditory pathway. These neurons are presumably part of the efferent tectal projection pathway that mediates head saccades. The implications of a sensory alignment signal possibly being delivered by a (pre)motor command pathway are discussed.

Throwing light on plasticity, with shades

The ability to localize sound in space is important for many species but it is vital for those that hunt in conditions of poor light. The alignment of auditory and visual maps necessary to achieve this function is performed in birds by neurons within the optic tectum that are tuned to respond to the location of an auditory stimulus. Under normal conditions, neurons in the optic tectum that respond to both auditory and visual stimuli have mutually aligned auditory and spatial visual fields. It is well known that during development this alignment can be disrupted radically by fitting prisms over the eyes. The prisms displace the visual information reaching the optic tectum and thus force a physiological adjustment to the auditory map to bring it into register with the displaced visual information. This capacity for readjustment is much reduced in adults. Eric Knudsen[1xCapacity for plasticity in the adult owl auditory system expanded by juvenile experience. Knudsen, E. Science. 1998; 279: 1531–1533Crossref | PubMed | Scopus (100)See all References[1]has recently demonstrated that despite this apparent reduced plasticity, the adult system does retain some plasticity in certain circumstances. Thus, Knudsen found that while naive adult barn owls were unable to re-tune their auditory maps when prisms were placed over their eyes, adult birds that had previously experienced the prisms when younger could do so. Moveover, the re-tuning was limited to those directions or magnitudes of displacement that had been previously experienced during development. The results could suggest that reactivation of older connections occurred in the adult birds even though the birds had not experienced the prisms for the last 6 months. These results therefore provide valuable insight into the mechanisms controlling neuronal plasticity.

Neuroethological studies of cognitive and perceptual processes

* Introduction: Neuroethology, Perception, and Cognition Sara J. Shettleworth. Specializations In Learning * Specializations in Honey Bee Learning James L. Gould. * Detecting Associations in Pavlovian Conditioning and Instrumental Learning in Invertebrates and in Vertebrates Ruth M. Colwill. * Neuroethological Studies on How Birds Discriminate Song Jeffrey Cynx. * Ecological Specialization in the Avian Brain Susan D. Healy. Specializations For Perception Of Biologically Relevant Stimuli * The Perceptual Foundations of Adult Vocal Learning in Budgerigars Robert J. Dooling, Susan D. Brown, Kazuchika Manabe, and Elizabeth F. Powell. * How Birds Use Frequency to Recognize Their Songs Daniel M. Weary. * Development of Perceptual Mechanisms in Birds: Predispositions and Imprinting Johan J. Bolhuis. * Neural Codes for Pitch Processing in a Unique Vertebrate Auditory System Andrea M. Simmons and Rebecca C. Buxbaum. * Recognition of Visual Signals: Eyes Specialize Russell D. Fernald. Specializations For Spatial Perception And Orientation * Perception Along the Axis of Target Range in the Echolocating Bat Cynthia F. Moss and James A. Simmons. * Converging Approaches to Determining Sound Localization Mechanisms in the Big Brown Bat, Eptesicus fuscus Tim Haresign, Janine M. Wotton, Michael Ferragamo, and J. A. Simmons. * Sound Localization from Binaural Cues by the Barn Owl Auditory System Andrew Moiseff, T. Haresign, and Jianxin Wang.

Representation of interaural level difference in the VLVp, the first site of binaural comparison in the barn owl's auditory system

In the avian auditory system, the posterior division of the ventral nucleus of the lateral lemniscus (VLVp) is the first site where the levels of sound arriving at the two ears are compared. VLVp units are excited by sound at the contralateral ear and are inhibited by sound at the ipsilateral ear, and, as a result, are sensitive to interaural level differences (ILD). In this study, we investigate the functional properties of VLVp units and describe the topography of ILD sensitivity along the dorsoventral dimension of this nucleus. The responses of VLVp units were tested with monaural and binaural noise delivered through earphones. Excitatory and inhibitory responsiveness was quantified using several measures that assessed the effect of contra-ear stimulation and the effect of ipsi-ear stimulation on the contra-ear response. On the basis of these measures, we characterize the map of ILD sensitivity in the VLVp. The temporal pattern of unit responses were also analyzed. The discharges of VLVp units were regular and time-locked to the onset of a stimulus, a pattern of discharge reminiscent of the ‘chopper pattern’ observed in the lateral superior olive (LSO) of mammals. The temporal discharge patterns of a single VLVp neuron often distinguished between equivalent ILDs, resulting from different combinations of contra- and ipsi-ear levels, that were not distinguished by spike count alone. However, the temporal response pattern did not distinguish between all such combinations of contra- and ipsi-ear levels. The additional information was encoded by the pattern of activity across the entire population of VLVp neurons. This study describes similarities in the functional properties of VLVp and LSO units that suggest similar physiological mechanisms in avians and mammals for encoding similar acoustic information.

Owls with asymmetric ears: brain mechanisms of sound localization.

Barn owls localize sound most accurately among all animals. Studies on the brain mechanisms of their sound localization represent a case where many important questions in sensory physiology can be addressed in a straightforward way. This article will review our current understanding of how neurons in the owl's auditory system create their selectivity to position of sounds.

The role of GABAergic inhibition in processing of interaural time difference in the owl's auditory system

The barn owl uses interaural time differences (ITDs) to localize the azimuthal position of sound. ITDs are processed by an anatomically distinct pathway in the brainstem. Neuronal selectivity for ITD is generated in the nucleus laminaris (NL) and conveyed to both the anterior portion of the ventral nucleus of the lateral lemniscus (VLVa) and the central (ICc) and external (ICx) nuclei of the inferior colliculus. With tonal stimuli, neurons in all regions are found to respond maximally not only to the real ITD, but also to ITDs that differ by integer multiples of the tonal period. This phenomenon, phase ambiguity, does not occur when ICx neurons are stimulated with noise. The main aim of this study was to determine the role of GABAergic inhibition in the processing of ITDs. Selectivity for ITD is similar in the NL and VLVa and improves in the ICc and ICx. Iontophoresis of bicuculline methiodide (BMI), a selective GABAA antagonist, decreased the ITD selectivity of ICc and ICx neurons, but did not affect that of VLVa neurons. Responses of VLVa and ICc neurons to unfavorable ITDs were below the monaural response levels. BMI raised both binaural responses to unfavorable ITDs and monaural responses, though the former remained smaller than the latter. During BMI application, ICx neurons showed phase ambiguity to noise stimuli and no longer responded to a unique ITD. BMI increased the response magnitude and changed the temporal discharge patterns in the VLVa, ICc, and ICx. Iontophoretically applied GABA exerted effects opposite to those of BMI, and the effects could be antagonized with simultaneous application of BMI. These results suggest that GABAergic inhibition (1) sharpens ITD selectivity in the ICc and ICx, (2) contributes to the elimination of phase ambiguity in the ICx, and (3) controls response magnitude and temporal characteristics in the VLVa, ICc, and ICx. Through these actions, GABAergic inhibition shapes the horizontal dimension of the auditory receptive fields.

Auditory properties of space-tuned units in owl's optic tectum.

Auditory units in the optic tectum of the barn owl (Tyto alba) were studied under free-field conditions with a movable sound source. These units are selective for sound location and their spatial tuning varies systematically across the tectum, forming a map of space (8). I found that frequency tuning, response latencies, and thresholds of units changed in parallel with their spatial tuning, suggesting that as a consequence these properties also are topographically distributed in the optic tectum. Response rates were determined primarily by the location of the sound source. Regardless of sound intensity, only stimuli delivered from a restricted "best area" elicited vigorous responses. Minimum response latencies were shortest for units with frontal best areas and increased systematically for units with best areas located more peripherally. The response latencies of units with best areas centered within 25 degrees of the owl's visual axis were virtually independent of sound intensity and speaker position. The latencies of units with more peripheral best areas varied with speaker position and were shortest when the speaker was in the best area. Thresholds to noise stimuli were lowest for units with best areas directly in front of the owl and increased systematically for units with best areas located more peripherally. Thus, in the representation of frontal space, where units have the smallest receptive fields and the magnification of space is the greatest (8), units also respond to the weakest sound fields. Many units (20%) could not be driven with tonal stimuli; of those that could, most were broadly tuned for frequency. Characteristic frequencies and high-frequency cutoffs shifted lower as best areas moved peripherally. High-frequency tones, which excited units with frontal best areas, either inhibited or failed to drive units with peripheral best areas. These systematic changes in unit response properties influence how sounds from different locations are represented in the tectum and reflect integrative strategies used by the owl's auditory system in deriving a representation of auditory space.

Time and intensity cues are processed independently in the auditory system of the owl

Space-specific neurons, found in the barn owl's inferior colliculus, respond selectively to a narrow range of interaural time and intensity differences. We show that injecting a local anesthetic into one cochlear nucleus, nucleus magnocellularis, alters the space-specific cell's selectivity for interaural time difference, leaving its selectivity for interaural intensity difference intact. Anesthetizing the other cochlear nucleus, nucleus angularis, has the converse effects. We show also that the space-specific neuron's selectivity for one interaural cue is the same for all effective values of the other cue. We conclude that time and intensity cues are processed in separate neural channels of the barn owl's auditory system and that the two cues operate independently.