Bayesian models have proven effective in characterizing perception, behavior, and neural encoding across diverse species and systems. The neural implementation of Bayesian inference in the barn owl's ...sound localization system and behavior has been previously explained by a non-uniform population code model. This model specifies the neural population activity pattern required for a population vector readout to match the optimal Bayesian estimate. While prior analyses focused on trial-averaged comparisons of model predictions with behavior and single-neuron responses, it remains unknown whether this model can accurately approximate Bayesian inference on single trials under varying sensory reliability, a fundamental condition for natural perception and behavior. In this study, we utilized mathematical analysis and simulations to demonstrate that decoding a non-uniform population code via a population vector readout approximates the Bayesian estimate on single trials for varying sensory reliabilities. Our findings provide additional support for the non-uniform population code model as a viable explanation for the barn owl's sound localization pathway and behavior.
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DOBA, IZUM, KILJ, NUK, PILJ, PNG, SAZU, SIK, UILJ, UKNU, UL, UM, UPUK
The natural environment challenges the brain to prioritize the processing of salient stimuli. The barn owl, a sound localization specialist, exhibits a circuit called the midbrain stimulus selection ...network, dedicated to representing locations of the most salient stimulus in circumstances of concurrent stimuli. Previous competition studies using unimodal (visual) and bimodal (visual and auditory) stimuli have shown that relative strength is encoded in spike response rates. However, open questions remain concerning auditory-auditory competition on coding. To this end, we present diverse auditory competitors (concurrent flat noise and amplitude-modulated noise) and record neural responses of awake barn owls of both sexes in subsequent midbrain space maps, the external nucleus of the inferior colliculus (ICx) and optic tectum (OT). While both ICx and OT exhibit a topographic map of auditory space, OT also integrates visual input and is part of the global-inhibitory midbrain stimulus selection network. Through comparative investigation of these regions, we show that while increasing strength of a competitor sound decreases spike response rates of spatially distant neurons in both regions, relative strength determines spike train synchrony of nearby units only in the OT. Furthermore, changes in synchrony by sound competition in the OT are correlated to gamma range oscillations of local field potentials associated with input from the midbrain stimulus selection network. The results of this investigation suggest that modulations in spiking synchrony between units by gamma oscillations are an emergent coding scheme representing relative strength of concurrent stimuli, which may have relevant implications for downstream readout.
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
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.
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.
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.
Interaural time and level differences are important cues for sound localization. We wondered whether the broadband information contained in these two cues could fully explain the behavior of barn ...owls and responses of midbrain neurons in these birds. To tackle this problem, we developed a novel approach based on head-related transfer functions. These filters contain the complete information present at the eardrum. We selected positions in space characterized by equal broadband interaural time and level differences. Stimulation from such positions provides reduced information to the owl. We show that barn owls are able to discriminate between such positions. In many cases, but not all, the owls may have used spectral components of interaural level differences that exceeded the known behavioral resolution and variability for discrimination. Alternatively, the birds may have used template matching. Likewise, neurons in the optic tectum of the barn owl, a nucleus involved in sensorimotor integration, contained more information than is available in the broadband interaural time and level differences. Thus, these data show that more information is available and used by barn owls for sound localization than carried by broadband interaural time and level differences.
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.
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.
A function of the auditory system is to accurately determine the location of a sound source. The main cues for sound location are interaural time (ITD) and level (ILD) differences. Humans use both ...ITD and ILD to determine the azimuth. Thus far, the conception of sound localization in barn owls was that their facial ruff and asymmetrical ears generate a two-dimensional grid of ITD for azimuth and ILD for elevation. We show that barn owls also use ILD for azimuthal sound localization when ITDs are ambiguous. For high-frequency narrowband sounds, midbrain neurons can signal multiple locations, leading to the perception of an auditory illusion called a phantom source. Owls respond to such an illusory percept by orienting toward it instead of the true source. Acoustical measurements close to the eardrum reveal a small ILD component that changes with azimuth, suggesting that ITD and ILD information could be combined to eliminate the illusion. Our behavioral data confirm that perception was robust against ambiguities if ITD and ILD information was combined. Electrophysiological recordings of ILD sensitivity in the owl's midbrain support the behavioral findings indicating that rival brain hemispheres drive the decision to orient to either true or phantom sources. Thus, the basis for disambiguation, and reliable detection of sound source azimuth, relies on similar cues across species as similar response to combinations of ILD and narrowband ITD has been observed in humans.
The factors determining gradients of biodiversity are a fundamental yet unresolved topic in ecology. While diversity gradients have been analysed for numerous single taxa, progress towards general ...explanatory models has been hampered by limitations in the phylogenetic coverage of past studies. By parallel sampling of 25 major plant and animal taxa along a 3.7 km elevational gradient on Mt. Kilimanjaro, we quantify cross-taxon consensus in diversity gradients and evaluate predictors of diversity from single taxa to a multi-taxa community level. While single taxa show complex distribution patterns and respond to different environmental factors, scaling up diversity to the community level leads to an unambiguous support for temperature as the main predictor of species richness in both plants and animals. Our findings illuminate the influence of taxonomic coverage for models of diversity gradients and point to the importance of temperature for diversification and species coexistence in plant and animal communities.
The monitoring of species and functional diversity is of increasing relevance for the development of strategies for the conservation and management of biodiversity. Therefore, reliable estimates of ...the performance of monitoring techniques across taxa become important. Using a unique dataset, this study investigates the potential of airborne LiDAR-derived variables characterizing vegetation structure as predictors for animal species richness at the southern slopes of Mount Kilimanjaro. To disentangle the structural LiDAR information from co-factors related to elevational vegetation zones, LiDAR-based models were compared to the predictive power of elevation models. 17 taxa and 4 feeding guilds were modeled and the standardized study design allowed for a comparison across the assemblages. Results show that most taxa (14) and feeding guilds (3) can be predicted best by elevation with normalized RMSE values but only for three of those taxa and two of those feeding guilds the difference to other models is significant. Generally, modeling performances between different models vary only slightly for each assemblage. For the remaining, structural information at most showed little additional contribution to the performance. In summary, LiDAR observations can be used for animal species prediction. However, the effort and cost of aerial surveys are not always in proportion with the prediction quality, especially when the species distribution follows zonal patterns, and elevation information yields similar results.
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