Decoding neural responses to temporal cues for sound localization

The activity of sensory neural populations carries information about the environment. This may be extracted from neural activity using different strategies. In the auditory brainstem, a recent theory proposes that sound location in the horizontal plane is decoded from the relative summed activity of two populations in each hemisphere, whereas earlier theories hypothesized that the location was decoded from the identity of the most active cells. We tested the performance of various decoders of neural responses in increasingly complex acoustical situations, including spectrum variations, noise, and sound diffraction. We demonstrate that there is insufficient information in the pooled activity of each hemisphere to estimate sound direction in a reliable way consistent with behavior, whereas robust estimates can be obtained from neural activity by taking into account the heterogeneous tuning of cells. These estimates can still be obtained when only contralateral neural responses are used, consistently with unilateral lesion studies. DOI: http://dx.doi.org/10.7554/eLife.01312.001

Multiplicative Auditory Spatial Receptive Fields Created by a Hierarchy of Population Codes

A multiplicative combination of tuning to interaural time difference (ITD) and interaural level difference (ILD) contributes to the generation of spatially selective auditory neurons in the owl's midbrain. Previous analyses of multiplicative responses in the owl have not taken into consideration the frequency-dependence of ITD and ILD cues that occur under natural listening conditions. Here, we present a model for the responses of ITD- and ILD-sensitive neurons in the barn owl's inferior colliculus which satisfies constraints raised by experimental data on frequency convergence, multiplicative interaction of ITD and ILD, and response properties of afferent neurons. We propose that multiplication between ITD- and ILD-dependent signals occurs only within frequency channels and that frequency integration occurs using a linear-threshold mechanism. The model reproduces the experimentally observed nonlinear responses to ITD and ILD in the inferior colliculus, with greater accuracy than previous models. We show that linear-threshold frequency integration allows the system to represent multiple sound sources with natural sound localization cues, whereas multiplicative frequency integration does not. Nonlinear responses in the owl's inferior colliculus can thus be generated using a combination of cellular and network mechanisms, showing that multiple elements of previous theories can be combined in a single system

Coding of auditory space

Behavioral, anatomical, and physiological approaches can be integrated in the study of sound localization in barn owls. Space representation in owls provides a useful example for discussion of place and ensemble coding. Selectivity for space is broad and ambiguous in low-order neurons. Parallel pathways for binaural cues and for different frequency bands converge on high-order space-specific neurons, which encode space more precisely. An ensemble of broadly tuned place-coding neurons may converge on a single high-order neuron to create an improved labeled line. Thus, the two coding schemes are not alternate methods. Owls can localize sounds by using either the isomorphic map of auditory space in the midbrain or forebrain neural networks in which space is not mapped

Computation of Interaural Time Difference in the Owl's Coincidence Detector Neurons

Both the mammalian and avian auditory systems localize sound sources by computing the interaural time difference (ITD) with submillisecond accuracy. The neural circuits for this computation in birds consist of axonal delay lines and coincidence detector neurons. Here, we report the first in vivo intracellular recordings from coincidence detectors in the nucleus laminaris of barn owls. Binaural tonal stimuli induced sustained depolarizations (DC) and oscillating potentials whose waveforms reflected the stimulus. The amplitude of this sound analog potential (SAP) varied with ITD, whereas DC potentials did not. The amplitude of the SAP was correlated with firing rate in a linear fashion. Spike shape, synaptic noise, the amplitude of SAP, and responsiveness to current pulses differed between cells at different frequencies, suggesting an optimization strategy for sensing sound signals in neurons tuned to different frequencies

Dynamic plasticity in coupled avian midbrain maps

Internal mapping of the external environment is carried out using the receptive fields of topographic neurons in the brain, and in a normal barn owl the aural and visual subcortical maps are aligned from early experiences. However, instantaneous misalignment of the aural and visual stimuli has been observed to result in adaptive behavior, manifested by functional and anatomical changes of the auditory processing system. Using methods of information theory and statistical mechanics a model of the adaptive dynamics of the aural receptive field is presented and analyzed. The dynamics is determined by maximizing the mutual information between the neural output and the weighted sensory neural inputs, admixed with noise, subject to biophysical constraints. The reduced costs of neural rewiring, as in the case of young barn owls, reveal two qualitatively different types of receptive field adaptation depending on the magnitude of the audiovisual misalignment. By letting the misalignment increase with time, it is shown that the ability to adapt can be increased even when neural rewiring costs are high, in agreement with recent experimental reports of the increased plasticity of the auditory space map in adult barn owls due to incremental learning. Finally, a critical speed of misalignment is identified, demarcating the crossover from adaptive to nonadaptive behavior

Tolerance to Sound Intensity of Binaural Coincidence Detection in the Nucleus Laminaris of the Owl

Neurons of the owl's nucleus laminaris serve as coincidence detectors for measurement of interaural time difference. The discharge rate of nucleus laminaris neurons for both monaural and binaural stimulation increased with sound intensity until they reached an asymptote. Intense sounds affected neither the ratio between binaural and monaural responses nor the interaural time difference for which nucleus laminaris neurons were selective. Theoretical analysis showed that high afferent discharge rates cause coincidence detectors with only excitatory input to lose their selectivity for interaural time difference when coincidence of impulses from the same side becomes as likely as that of impulses from the two sides. We hypothesize that inhibitory input whose strength increases with sound intensity protects nucleus laminaris neurons from losing their sensitivity to interaural time difference with intense sounds

Modelling of human low frequency sound localization acuity demonstrates dominance of spatial variation of interaural time difference and suggests uniform just-noticeable differences in interaural time difference.

Sound source localization is critical to animal survival and for identification of auditory objects. We investigated the acuity with which humans localize low frequency, pure tone sounds using timing differences between the ears. These small differences in time, known as interaural time differences or ITDs, are identified in a manner that allows localization acuity of around 1° at the midline. Acuity, a relative measure of localization ability, displays a non-linear variation as sound sources are positioned more laterally. All species studied localize sounds best at the midline and progressively worse as the sound is located out towards the side. To understand why sound localization displays this variation with azimuthal angle, we took a first-principles, systemic, analytical approach to model localization acuity. We calculated how ITDs vary with sound frequency, head size and sound source location for humans. This allowed us to model ITD variation for previously published experimental acuity data and determine the distribution of just-noticeable differences in ITD. Our results suggest that the best-fit model is one whereby just-noticeable differences in ITDs are identified with uniform or close to uniform sensitivity across the physiological range. We discuss how our results have several implications for neural ITD processing in different species as well as development of the auditory system

Ergodicity breaking and lack of a typical waiting time in area-restricted search of avian predators

Movement tracks of wild animals frequently fit models of anomalous rather than simple diffusion, mostly reported as ergodic superdiffusive motion combining area-restricted search within a local patch and larger-scale commuting between patches, as highlighted by the L\'evy walk paradigm. Since L\'evy walks are scale invariant, superdiffusive motion is also expected within patches, yet investigation of such local movements has been precluded by the lack of accurate high-resolution data at this scale. Here, using rich high-resolution movement datasets ($>\! 7 \times 10^7$ localizations) from 70 individuals and continuous-time random walk modeling, we found subdiffusive behavior and ergodicity breaking in the localized movement of three species of avian predators. Small-scale, within-patch movement was qualitatively different, not inferrable and separated from large-scale inter-patch movement via a clear phase transition. Local search is characterized by long power-law-distributed waiting times with diverging mean, giving rise to ergodicity breaking in the form of considerable variability uniquely observed at this scale. This implies that wild animal movement is scale specific rather than scale free, with no typical waiting time at the local scale. Placing these findings in the context of the static-ambush to mobile-cruise foraging continuum, we verify predictions based on the hunting behavior of the study species and the constraints imposed by their prey.Comment: 27 pages, 8 figure