Disproportionate Frequency Representation in the Inferior Colliculus of Doppler-Compensating Greater Horseshoe Bats. Evidence for an Acoustic Fovea

1. The inferior colliculus of 8 Greater Horseshoe bats (Rhinolophus ferrumequinun) was systematically sampled with electrode penetrations covering the entire volume of the nucleus. The best frequencies and intensity thresholds for pure tones (Fig. 2) were determined for 591 neurons. The locations of the electrode penetrations within the inferior colliculus were histologically verified. 2. About 50% of all neurons encountered had best frequencies (BF) in the frequency range between 78 and 88 kHz (Table 1, Fig. 1A). Within this frequency range the BFs between 83.0 and 84.5 kHz were overrepresented with 16.3% of the total population of neurons (Fig. 1B). The frequencies of the constant frequency components of the echoes fall into this frequency range. 3. The representation of BFs expressed as number of neurons per octave shows a striking correspondence to the nonuniform innervation density in the afferent innervation of the basilar membrane (Bruns and Schmieszek, in press). The high innervation density of the basilar membrane in the frequency band between 83 and 84.5 kHz coincides with the maximum of the distribution of number of neurons per octave across frequency in the inferior colliculus (Fig. 1 C). 4. The disproportionate representation of frequencies in the auditory system of the greater horseshoe bat is described as an acoustical fovea functioning in analogy to the fovea in the visual system. The functional importance of the Doppler-shift compensation for such a foveal mechanism in the auditory system of horseshoe bats is related to that of tracking eye movements in the visual system

Neural delays shape selectivity to interaural intensity differences in the lateral superior olive

Neurons in the lateral superior olive (LSO) respond selectively to interaural intensity differences (IIDs), one of the chief cues used to localize sounds in space. LSO cells are innervated in a characteristic pattern: they receive an excitatory input from the ipsilateral ear and an inhibitory input from the contralateral ear. Consistent with this pattern, LSO cells generally are excited by sounds that are more intense at the ipsilateral ear and inhibited by sounds that are more intense at the contralateral ear. Despite their relatively homogeneous pattern of innervation, IID selectivity varies substantially from cell to cell, such that selectivities are distributed over the range of IIDs that would be encountered in nature. For some time, researchers have speculated that the relative timing of the excitatory and inhibitory inputs to an LSO cell might shape IID selectivity. To test this hypothesis, we recorded from 50 LSO cells in the free-tailed bat while presenting stimuli that varied in interaural intensity and in interaural time of arrival. The results suggest that, for more than half of the cells, the latency of inhibition was several hundred microseconds longer than the latency of excitation. Increasing the intensity to the inhibitory ear shortened the latency of inhibition and brought the timing of the inputs from the two ears into register. Thus, a neural delay of the inhibition helped to define the IID selectivity of these cells, accounting for a significant part of the variation in selectivity among LSO cells

Inhibiting the inhibition

The precedence effect describes the phenomenon whereby echoes are spatially fused to the location of an initial sound by selectively suppressing the directional information of lagging sounds (echo suppression). Echo suppression is a prerequisite for faithful sound localization in natural environments but can break down depending on the behavioral context. To date, the neural mechanisms that suppress echo directional information without suppressing the perception of echoes themselves are not understood. We performed in vivo recordings in Mongolian gerbils of neurons of the dorsal nucleus of the lateral lemniscus (DNLL), a GABAergic brainstem nucleus that targets the auditory midbrain, and show that these DNLL neurons exhibit inhibition that persists tens of milliseconds beyond the stimulus offset, so-called persistent inhibition (PI). Using in vitro recordings, we demonstrate that PI stems from GABAergic projections from the opposite DNLL. Furthermore, these recordings show that PI is attributable to intrinsic features of this GABAergic innervation. Implementation of these physiological findings into a neuronal model of the auditory brainstem demonstrates that, on a circuit level, PI creates an enhancement of responsiveness to lagging sounds in auditory midbrain cells. Moreover, the model revealed that such response enhancement is a sufficient cue for an ideal observer to identify echoes and to exhibit echo suppression, which agrees closely with the percepts of human subjects

Inhibitory projections from the ventral nucleus of the lateral lemniscus and superior paraolivary nucleus create directional selectivity of frequency modulations in the inferior colliculus: A comparison of bats with other mammals

This review considers four auditory brainstem nuclear groups and shows how studies of both bats and other mammals have provided insights into their response properties and the impact of their convergence in the inferior colliculus (IC). The four groups are octopus cells in the cochlear nucleus, their connections with the ventral nucleus of the lateral lemniscus (VNLL) and the superior paraolivary nucleus (SPON), and the connections of the VNLL and SPON with the IC. The theme is that the response properties of neurons in the SPON and VNLL map closely onto the synaptic response features of a unique subpopulation of cells in the IC of bats whose inputs are dominated by inhibition. We propose that the convergence of VNLL and SPON inputs generates the tuning of these IC cells, their unique temporal responses to tones, and their directional selectivities for frequency modulated (FM) sweeps. Other IC neurons form directional properties in other ways, showing that selective response properties are formed in multiple ways. In the final section we discuss why multiple formations of common response properties could amplify differences in population activity patterns evoked by signals that have similar spectrotemporal features

The dominance of inhibition in the inferior colliculus

Almost all of the processing that occurs in the various lower auditory nuclei converges upon a common target in the central nucleus of the inferior colliculus (ICc) thus making the ICc the nexus of the auditory system. A variety of new response properties are formed in the ICc through the interactions among the excitatory and inhibitory inputs that converge upon it. Here we review studies that illustrate the dominant role inhibition plays in the ICc. We begin by reviewing studies of tuning curves and show how inhibition shapes the variety of tuning curves in the ICc through sideband inhibition. We then show how inhibition shapes selective response properties for complex signals, focusing on selectivity for the sweep direction of frequency modulations (FM). In the final section we consider results from in vivo whole-cell recordings that show how parameters of the incoming excitation and inhibition interact to shape directional selectivity. We show that post-synaptic potentials (PSPs) evoked by different signals can be similar but evoke markedly different spike-counts. In these cases, spike threshold acts as a non-linear amplifier that converts small differences in PSPs into large differences in spike output. Such differences between the inputs to a cell compared to the outputs from the same cell suggest that highly selective discharge properties can be created by only minor adjustments in the synaptic strengths evoked by one or both signals. These findings also suggest that plasticity of response features may be achieved with far less modifications in circuitry than previously supposed

Numerical Comparison of Cusum and Shiryaev-Roberts Procedures for Detecting Changes in Distributions

The CUSUM procedure is known to be optimal for detecting a change in distribution under a minimax scenario, whereas the Shiryaev-Roberts procedure is optimal for detecting a change that occurs at a distant time horizon. As a simpler alternative to the conventional Monte Carlo approach, we propose a numerical method for the systematic comparison of the two detection schemes in both settings, i.e., minimax and for detecting changes that occur in the distant future. Our goal is accomplished by deriving a set of exact integral equations for the performance metrics, which are then solved numerically. We present detailed numerical results for the problem of detecting a change in the mean of a Gaussian sequence, which show that the difference between the two procedures is significant only when detecting small changes.Comment: 21 pages, 8 figures, to appear in Communications in Statistics - Theory and Method

Demography and mating system shape the genome-wide impact of purifying selection in Arabis alpina

YesPlant mating systems have profound effects on levels and structuring of genetic variation and can affect the impact of natural selection. Although theory predicts that intermediate outcrossing rates may allow plants to prevent accumulation of deleterious alleles, few studies have empirically tested this prediction using genomic data. Here, we study the effect of mating system on purifying selection by conducting population-genomic analyses on whole-genome resequencing data from 38 European individuals of the arctic-alpine crucifer Arabis alpina. We find that outcrossing and mixed-mating populations maintain genetic diversity at similar levels, whereas highly self-fertilizing Scandinavian A. alpina show a strong reduction in genetic diversity, most likely as a result of a postglacial colonization bottleneck. We further find evidence for accumulation of genetic load in highly self-fertilizing populations, whereas the genome-wide impact of purifying selection does not differ greatly between mixed-mating and outcrossing populations. Our results demonstrate that intermediate levels of outcrossing may allow efficient selection against harmful alleles, whereas demographic effects can be important for relaxed purifying selection in highly selfing populations. Thus, mating system and demography shape the impact of purifying selection on genomic variation in A. alpina. These results are important for an improved understanding of the evolutionary consequences of mating system variation and the maintenance of mixed-mating strategies.This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1707492115/-/DCSupplemental

Versatility and Stereotypy of Free-Tailed Bat Songs

In mammals, complex songs are uncommon and few studies have examined song composition or the order of elements in songs, particularly with respect to regional and individual variation. In this study we examine how syllables and phrases are ordered and combined, ie “syntax”, of the song of Tadarida brasiliensis, the Brazilian free-tailed bat. Specifically, we test whether phrase and song composition differ among individuals and between two regions, we determine variability across renditions within individuals, and test whether phrases are randomly ordered and combined. We report three major findings. First, song phrases were highly stereotyped across two regions, so much so that some songs from the two colonies were almost indistinguishable. All males produced songs with the same four types of syllables and the same three types of phrases. Second, we found that although song construction was similar across regions, the number of syllables within phrases, and the number and order of phrases in songs varied greatly within and among individuals. Last, we determined that phrase order, although diverse, deviated from random models. We found broad scale phrase-order rules and certain higher order combinations that were highly preferred. We conclude that free-tailed bat songs are composed of highly stereotyped phrases hierarchically organized by a common set of syntactical rules. However, within global species-specific patterns, songs male free-tailed bats dynamically vary syllable number, phrase order, and phrase repetitions across song renditions