Auditory temporal resolution and evoked responses to pulsed sounds for the Yangtze finless porpoises (<Emphasis Type="Italic">Neophocaena phocaenoides asiaeorientalis</Emphasis>)

Temporal cues are important for some forms of auditory processing, such as echolocation. Among odontocetes (toothed whales, dolphins, and porpoises), it has been suggested that porpoises may have temporal processing abilities which differ from other odontocetes because of their relatively narrow auditory filters and longer duration echolocation signals. This study examined auditory temporal resolution in two Yangtze finless porpoises (Neophocaena phocaenoides asiaeorientalis) using auditory evoked potentials (AEPs) to measure: (a) rate following responses and modulation rate transfer function for 100 kHz centered pulse sounds and (b) hearing thresholds and response amplitudes generated by individual pulses of different durations. The animals followed pulses well at modulation rates up to 1,250 Hz, after which response amplitudes declined until extinguished beyond 2,500 Hz. The subjects had significantly better hearing thresholds for longer, narrower-band pulses similar to porpoise echolocation signals compared to brief, broadband sounds resembling dolphin clicks. Results indicate that the Yangtze finless porpoise follows individual acoustic signals at rates similar to other odontocetes tested. Relatively good sensitivity for longer duration, narrow-band signals suggests that finless porpoise hearing is well suited to detect their unique echolocation signals.     

Some comments on the proposed perception of phase and nanosecond time disparities by echolocating bats

In a series of recent reports, Simmons and his colleagues propose that bats are able to accurately encode the spectral, temporal and phase information of their emitted calls and echoes. The information so encoded is then extracted by the networks of the auditory system with specialized processing. They propose that bats use this information to determine the distance to their target by crosscorrelating the entire structure of the emitted call with the structure of the echo. The idea is that slight deviations in the correlation function can be detected by the bat and the degree of mismatch provides an accurate measure of temporal disparity and hence range. The data in the reports purport to show that bats perceive the phase of ultrasonic signals and that they can resolve temporal disparities of about 10 ns, and thus can distinguish range differences as small as 2 m.The hypothesis also attempts to explain how a variety of acoustic cues are processed and represented in the auditory system and how they are combined to form a unitary percept of space and fine structure. The theory incorporates some time honored processes of extracting information, such as crosscorrelations. The implications of. the hypothesis, however, go far beyond a theory of neural processing and representation of information by ensembles of cells. The hypothesis requires some remarkable abilities, such as the phase coding of ultrasonic signals and a temporal acuity on the order of 10 ns. These features have never been seen in any neurophysiological study of any animal nor has its existence been implied in behavioral studies of other animals. If bats, in fact, detect and process those signals in the manner proposed by Simmons and his colleagues, it would suggest that bats are supermammals whose auditory systems have evolved new and extraordinary mechanisms not possessed by other animals.In view of the extraordinary implications of the hypothesis, it seems prudent to critically evaluate the data upon which the hypothesis is based. The purpose of this review is to point out a number of technical problems and deficiencies in those experiments which undermine the veracity of the purported demonstration of phase perception and nanosecond time resolution by bats.     

Variability of spike trains and the processing of temporal patterns of acoustic signals—problems,constraints, and solutions

Object recognition and classification by sensory pathways is rooted in spike trains provided by sensory neurons. Nervous systems had to evolve mechanisms to extract information about relevant object properties, and to separate these from spurious features. In this review, problems caused by spike train variability and counterstrategies are exemplified for the processing of acoustic signals in orthopteran insects. Due to size limitations of their nervous system we expect to find solutions that are stripped to the computational basics. A key feature of auditory systems is temporal resolution, which is likely limited by spike train variability. Basic strategies to reduce such variability are to integrate over time, or to average across several neurons. The first strategy is constrained by its possible interference with temporal resolution. Grasshoppers do not seem to explore temporal integration much, in spite of the repetitive structure of their songs, which invites for multiple looks at the signal. The benefits of averaging across neurons depend on uncorrelated responses, a factor that may be crucial for the performance and evolution of small nervous systems. In spite of spike train variability the temporal information necessary for the recognition of conspecifics is preserved to a remarkable degree in the auditory pathway.Abbreviations dB decibel - CV coefficient of variation - SNR signal to noise ratio     

Intensity invariance properties of auditory neurons compared to the statistics of relevant natural signals in grasshoppers

The temporal pattern of amplitude modulations (AM) is often used to recognize acoustic objects. To identify objects reliably, intensity invariant representations have to be formed. We approached this problem within the auditory pathway of grasshoppers. We presented AM patterns modulated at different time scales and intensities. Metric space analysis of neuronal responses allowed us to determine how well, how invariantly, and at which time scales AM frequency is encoded. We find that in some neurons spike-count cues contribute substantially (20–60%) to the decoding of AM frequency at a single intensity. However, such cues are not robust when intensity varies. The general intensity invariance of the system is poor. However, there exists a range of AM frequencies around 83 Hz where intensity invariance of local interneurons is relatively high. In this range, natural communication signals exhibit much variation between species, suggesting an important behavioral role for this frequency band. We hypothesize, just as has been proposed for human speech, that the communication signals might have evolved to match the processing properties of the receivers. This contrasts with optimal coding theory, which postulates that neuronal systems are adapted to the statistics of the relevant signals.     

Innovative biomechanics for directional hearing in small flies

In humans and animals alike, the localization of sound constitutes a fundamental processing task of the auditory system. Directional hearing relies on acoustic cues such as the interaural amplitude and time differences and also, sometimes, the signal spectral composition. In small animals, such as insects, the auditory receptors are forcibly set close together, a design constraint imposing very short interaural distances. Due to the physics of sound propagation, the close proximity of the sound receivers results in vanishingly small amplitude and time cues. Yet, because of their directionality, small auditory systems embed original and innovative solutions that can be of inspirational value to some acute problems of technological miniaturization. Such ears are found in a parasitoid fly that acoustically locates its singing cricket host. Anatomically rather unconventional, the fly's auditory system is endowed with a directional sensitivity that is based on the mechanical coupling between its two hemilateral tympanal membranes. The functional principle permitting this directionality may be of particular relevance for technological applications necessitating sensors that are low cost, low weight, and low energy. Based on silicon-etching technology, early prototypes of sub-millimeter acoustic sensors provide evidence for directional mechanical responses. Further developments hold the promise of applications in hearing aid technology, vibration sensors, and miniature video-acoustic surveillance systems.     

Evolutionary diversification of the auditory organ sensilla in Neoconocephalus katydids (Orthoptera: Tettigoniidae) correlates with acoustic signal diversification over phylogenetic relatedness and life history

Neoconocephalus Tettigoniidae are a model for the evolution of acoustic signals as male calls have diversified in temporal structure during the radiation of the genus. The call divergence and phylogeny in Neoconocephalus are established, but in tettigoniids in general, accompanying evolutionary changes in hearing organs are not studied. We investigated anatomical changes of the tympanal hearing organs during the evolutionary radiation and divergence of intraspecific acoustic signals. We compared the neuroanatomy of auditory sensilla (crista acustica) from nine Neoconocephalus species for the number of auditory sensilla and the crista acustica length. These parameters were correlated with differences in temporal call features, body size, life histories and different phylogenetic positions. By this, adaptive responses to shifting frequencies of male calls and changes in their temporal patterns can be evaluated against phylogenetic constraints and allometry. All species showed well‐developed auditory sensilla, on average 32–35 between species. Crista acustica length and sensillum numbers correlated with body size, but not with phylogenetic position or life history. Statistically significant correlations existed also with specific call patterns: a higher number of auditory sensilla occurred in species with continuous calls or slow pulse rates, and a longer crista acustica occurred in species with double pulses or slow pulse rates. The auditory sensilla show significant differences between species despite their recent radiation, and morphological and ecological similarities. This indicates the responses to natural and sexual selection, including divergence of temporal and spectral signal properties. Phylogenetic constraints are unlikely to limit these changes of the auditory systems.     

Hearing and frequency dependence of auditory interneurons in the parasitoid fly <Emphasis Type="Italic">Homotrixa alleni</Emphasis> (Tachinidae: Ormiini)

The parasitoid tachinid fly Homotrixa alleni detects its hosts by their acoustic signals. The tympanal organ of the fly is located at the prothorax and contains scolopidial sensory units of different size and orientation. The tympanal membrane vibrates in the frequency range of approximately 4–35 kHz, which is also reflected in the hearing threshold measured at the neck connective. The auditory organ is not tuned to the peak frequency (5 kHz) of the main host, the bush cricket Sciarasaga quadrata. Auditory afferents project in the three thoracic neuromeres. Most of the ascending interneurons branch in all thoracic neuromeres and terminate in the deutocerebrum of the brain. The interneurons do not differ considerably in frequency tuning, but in their sensitivity with lowest thresholds around 30 dB SPL. Suprathreshold responses of most neurons depend on frequency and intensity, indicating inhibitory influence at higher intensities. Some neurons respond particularly well at low frequency sounds (around 5 kHz) and high intensities (80–90 dB SPL), and thus may be involved in detection of the primary host, S. quadrata. The auditory system of H. alleni contains auditory interneurons reacting in a wide range of temporal patterns from strictly phasic to tonic and with clear differences in frequency responses.     

Auditory temporal resolution of a wild white-beaked dolphin (<Emphasis Type="Italic">Lagenorhynchus albirostris</Emphasis>)

Adequate temporal resolution is required across taxa to properly utilize amplitude modulated acoustic signals. Among mammals, odontocete marine mammals are considered to have relatively high temporal resolution, which is a selective advantage when processing fast traveling underwater sound. However, multiple methods used to estimate auditory temporal resolution have left comparisons among odontocetes and other mammals somewhat vague. Here we present the estimated auditory temporal resolution of an adult male white-beaked dolphin, (Lagenorhynchus albirostris), using auditory evoked potentials and click stimuli. Ours is the first of such studies performed on a wild dolphin in a capture-and-release scenario. The white-beaked dolphin followed rhythmic clicks up to a rate of approximately 1,125–1,250 Hz, after which the modulation rate transfer function (MRTF) cut-off steeply. However, 10% of the maximum response was still found at 1,450 Hz indicating high temporal resolution. The MRTF was similar in shape and bandwidth to that of other odontocetes. The estimated maximal temporal resolution of white-beaked dolphins and other odontocetes was approximately twice that of pinnipeds and manatees, and more than ten-times faster than humans and gerbils. The exceptionally high temporal resolution abilities of odontocetes are likely due primarily to echolocation capabilities that require rapid processing of acoustic cues.     

Noise filtering in the auditory system of Locusta migratoria L

Many acoustically communicating grasshoppers live in crowded populations where sound of many individuals may cause permanent noise. Tympanic receptors and first-order auditory interneurons of Locusta migratoria code such noise tonically, whereas many higher order interneurons react only weakly. In response to simultaneously presented sound they exhibit a better signal-to-noise ratio than their presynaptic elements. Two possible filter mechanisms are suggested for noise reduction in higher-order interneurons: (i) high-pass filtering of receptor spike frequencies and (ii) filtering due to synchronization of receptor spikes. Different receptor spike frequencies were elicited by series of short noise pulses with variable repetition rates. Receptor activities differing in their degree of synchronization were elicited by sound stimuli with variable rising times. In contrast to the first order interneurons some higher order interneurons responded best to receptor spike frequencies above 150–200 Hz, thus showing the postulated filtering. Only one higher order interneuron (AN4) distinguished between synchronous and asynchronous receptor activities. It is suggested that high-pass filtering of receptor spike frequencies is responsible for the noise filtering observed in these interneurons. The synchronization selectivity of AN4 is proposed to be responsible for temporal pattern detection of conspecific sounds.     

Spectrum of the calling songs, phonotaxis and the auditory system in the cricket Gryllus bimaculatus]

Behavioural experiments with Y-maze showed that phonotaxis in female crickets to male calling songs (CS) depends on the spectrum of the latter. Conservation of the first low-frequency (5 kc. p. s.) component of the spectrum is the necessary and sufficient condition for the development of normal phonotaxis. Signals which in their temporal characteristics are identical to the CS, but their spectrum contains only high-frequency (12.5 kc. p. s.) component, do no evoke positive phonotaxis. High-frequency signals (10-40 kc. p. s.) induce negative phonotaxis of females in the stationary flight. Beginning from the tympanic organ, the auditory system of crickets exhibits distinct differentiation of elements, which provide the analysis of low- and high-frequency signals. Two types of ascending interneurons transmitting information about the sound from the first auditory center to the brain were described in detail. The first type is associated mainly with low-frequency receptors and effectively transmits all that is necessary for the recognition of temporal characteristics of the CS. The second type presumably accounts for the negative phonotaxis. It is associated mainly with high-frequency receptors, exhibits for the negative phonotaxis. It is associated mainly with high-frequency receptors, exhibits significant after-effect, higher sensitivity to sounds of weak intensities, emphasizes the onset of the stimulus effect, and rapidly habituates to repetitive stimulation.     

听觉皮层信号处理

听觉系统和视觉系统的不同之处在于：听觉系统在外周感受器和听皮层间具有更长的皮层下通路和更多的突触联系。该特殊结构反应了听觉系统从复杂听觉环境中提取与行为相关信号的机制与其他感觉系统不同。听皮层神经信号处理包括两种重要的转换机制,声音信号的非同构转换以及从声音感受到知觉层面的转换。听觉皮层神经编码机制同时也受到听觉反馈和语言或发声过程中发声信号的调控。听觉神经科学家和生物医学工程师所面临的挑战便是如何去理解大脑中这些转换的编码机制。我将会用我实验室最近的一些发现来阐述听觉信号是如何在原听皮层中进行处理的,并讨论其对于言语和音乐在大脑中的处理机制以及设计神经替代装置诸如电子耳蜗的意义。我们使用了结合神经电生理技术和量化工程学的方法来研究这些问题。     

Temperature effects on the tympanal membrane and auditory receptor neurons in the locust

Poikilothermic animals are affected by variations in environmental temperature, as the basic properties of nerve cells and muscles are altered. Nevertheless, insect sensory systems, such as the auditory system, need to function effectively over a wide range of temperatures, as sudden changes of up to 10 °C or more are common. We investigated the performance of auditory receptor neurons and properties of the tympanal membrane of Locusta migratoria in response to temperature changes. Intracellular recordings of receptors at two temperatures (21 and 28 °C) revealed a moderate increase in spike rate with a mean Q10 of 1.4. With rising temperature, the spike rate–intensity–functions exhibited small decreases in thresholds and expansions of the dynamic range, while spike durations decreased. Tympanal membrane displacement, investigated using microscanning laser vibrometry, exhibited a small temperature effect, with a Q10 of 1.2. These findings suggest that locusts are affected by shifts in temperature at the periphery of the auditory pathway, but the effects on spike rate, sensitivity, and tympanal membrane displacement are small. Robust encoding of acoustic signals by only slightly temperature-dependent receptor neurons and almost temperature-independent tympanal membrane properties might enable locusts and grasshoppers to reliably identify sounds in spite of changes of their body temperature.     

Influence of sound pressure level on the processing of amplitude modulations by auditory neurons of the locust

Typical features of natural sounds are amplitude changes at different time scales. In many species, amplitude modulations constitute decisive cues to recognize communication signals. Since these signals should be recognizable over a broad intensity range, we investigated how the encoding of amplitude modulations by auditory neurons depends on sound pressure level. Identified neurons that represent different processing stages in the locusts’ auditory pathway were stimulated with sinusoidal modulations of a broad band noise carrier, at different intensities, and characteristic parameters of modulation transfer functions (MTFs) were determined. The corner frequencies of temporal MTFs turned out to be independent of intensity for all neurons except one. Furthermore, for none of the neurons investigated corner frequencies were significantly correlated with spike rate, indicating a remarkable intensity invariance of the upper limits of temporal resolution. The shape of the tMTFs changed with increasing intensity from a low-pass to a band-pass for receptors and local neurons, while no consistent change was observed for ascending neurons. The best modulation frequency depended on intensity and spike rate, especially for receptors and local neurons. Remarkably, the adaptation state of some neurons turned out to be independent of the spike rate during the modulation part of the stimulus.     

Neuronal identification of acoustic signal periodicity

Acoustic signals transmit information by temporal characteristics and envelope periodicity as well as by their frequency content. Many animals can extract the frequency content of a signal by means of specialized organs such as the cochlea but for the detection and identification of higher-order periodicity, e.g., amplitude modulations, this type of organ is useless. In addition, many animals do not have a cochlea but still depend on a reliable identification of different frequencies in the vast variety of acoustic signals they perceive in their natural environment. Hence, neural mechanisms to decode periodicity information must exist. We present a detailed mathematical analysis of a recurrent and a feedforward model of neuronal periodicity extraction and discuss basic constraints for neuronal circuitry performing such a task in a biological system. Both the recurrent and the feedforward model perform well using neuronal parameters typical for the auditory system. Performance is limited mainly by the temporal precision of the connections between the neurons.     

Temporal population code of concurrent vocal signals in the auditory midbrain

Unique patterns of spike activity across neuron populations have been implicated in the coding of complex sensory stimuli. Delineating the patterns of neural activity in response to varying stimulus parameters and their relationships to the tuning characteristics of individual neurons is essential to ascertaining the nature of population coding within the brain. Here, we address these points in the midbrain coding of concurrent vocal signals of a sound-producing fish, the plainfin midshipman. Midshipman produce multiharmonic vocalizations which frequently overlap to produce beats. We used multivariate statistical analysis from single-unit recordings across multiple animals to assess the presence of a temporal population code. Our results show that distinct patterns of temporal activity emerge among midbrain neurons in response to concurrent signals that vary in their difference frequency. These patterns can serve to code beat difference frequencies. The patterns directly result from the differential temporal coding of difference frequency by individual neurons. Difference frequency encoding, based on temporal patterns of activity, could permit the segregation of concurrent vocal signals on time scales shorter than codes requiring averaging. Given the ubiquity across vertebrates of auditory midbrain tuning to the temporal structure of acoustic signals, a similar temporal population code is likely present in other species.     

Structural Changes and Lack of HCN1 Channels in the Binaural Auditory Brainstem of the Naked Mole-Rat (Heterocephalus glaber)

Naked mole-rats (Heterocephalus glaber) live in large eu-social, underground colonies in narrow burrows and are exposed to a large repertoire of communication signals but negligible binaural sound localization cues, such as interaural time and intensity differences. We therefore asked whether monaural and binaural auditory brainstem nuclei in the naked mole-rat are differentially adjusted to this acoustic environment. Using antibody stainings against excitatory and inhibitory presynaptic structures, namely the vesicular glutamate transporter VGluT1 and the glycine transporter GlyT2 we identified all major auditory brainstem nuclei except the superior paraolivary nucleus in these animals. Naked mole-rats possess a well structured medial superior olive, with a similar synaptic arrangement to interaural-time-difference encoding animals. The neighboring lateral superior olive, which analyzes interaural intensity differences, is large and elongated, whereas the medial nucleus of the trapezoid body, which provides the contralateral inhibitory input to these binaural nuclei, is reduced in size. In contrast, the cochlear nucleus, the nuclei of the lateral lemniscus and the inferior colliculus are not considerably different when compared to other rodent species. Most interestingly, binaural auditory brainstem nuclei lack the membrane-bound hyperpolarization-activated channel HCN1, a voltage-gated ion channel that greatly contributes to the fast integration times in binaural nuclei of the superior olivary complex in other species. This suggests substantially lengthened membrane time constants and thus prolonged temporal integration of inputs in binaural auditory brainstem neurons and might be linked to the severely degenerated sound localization abilities in these animals.     

Auditory temporal computation: interval selectivity based on post-inhibitory rebound

The measurement of time is fundamental to the perception of complex, temporally structured acoustic signals such as speech and music, yet the mechanisms of temporal sensitivity in the auditory system remain largely unknown. Recently, temporal feature detectors have been discovered in several vertebrate auditory systems. For example, midbrain neurons in the fish Pollimyrus are activated by specific rhythms contained in the simple sounds they use for communication. This poses the significant challenge of uncovering the neuro-computational mechanisms that underlie temporal feature detection. Here we describe a model network that responds selectively to temporal features of communication sounds, yielding temporal selectivity in output neurons that matches the selectivity functions found in the auditory system of Pollimyrus. The output of the network depends upon the timing of excitatory and inhibitory input and post-inhibitory rebound excitation. Interval tuning is achieved in a behaviorally relevant range (10 to 40 ms) using a biologically constrained model, providing a simple mechanism that is suitable for the neural extraction of the relatively long duration temporal cues (i.e. tens to hundreds of ms) that are important in animal communication and human speech.     

A gain-control mechanism for processing of chorus sounds in the afferent auditory pathway of the bushcricket Tettigonia viridissima (Orthoptera; Tettigoniidae)

The representation of alternative conspecific acoustic signals in the responses of a pair of local interneurons of the bushcricket Tettigonia viridissima was studied with variation in intensity and the direction of sound signals. The results suggest that the auditory world of the bushcricket is rather sharply divided into two azimuthal hemispheres, with signals arriving from any direction within one hemisphere being predominantly represented in the discharge of neurons of this side of the auditory pathway. In addition, each pathway also selects for the most intense of several alternative sounds. A low-intensity signal at 45 dB sound pressure level is quite effective when presented alone, but completely suppressed when given simultaneously with another signal at 60 dB sound pressure level. In a series of intracellular experiments the synaptic nature of the intensity-dependent suppression of competitive signals was investigated in a number of interneurons. The underlying synaptic mechanism is based on a membrane hyperpolarisation with a time-constant in the order of 5–10 s. The significance of this mechanism for hearing in choruses, and for the evolution of acoustic signals and signalling behaviour is discussed. Accepted: 20 November 1999     

Changes in the auditory system of locusts (Locusta migratoria and Schistocerca gregaria) after deafferentation

Deafferentation experiments during postembryonic development show morphological and/or physiological changes of receptor fibers and of identified auditory interneurons in the CNS of the locusts Locusta migratoria and Schistocerca gregaria after unilateral ablation of one tympanic organ either in the larva or the adult animal.

Temporal modulation transfer functions in auditory receptor fibres of the locust (Locusta migratoria L.)

The temporal resolution of auditory receptors of locusts was investigated by applying noise stimuli with sinusoidal amplitude modulations and by computing temporal modulation transfer functions. These transfer functions showed mostly bandpass characteristics, which are rarely found in other species at the level of receptors. From the upper cut-off frequencies of the modulation transfer functions the minimum integration times were calculated. Minimum integration times showed no significant correlation to the receptor spike rates but depended strongly on the body temperature. At 20 degrees C the average minimum integration time was 1.7 ms, dropping to 0.95 ms at 30 degrees C. The values found in this study correspond well to the range of minimum integration times found in birds and mammals. Gap detection is another standard paradigm to investigate temporal resolution. In locusts and other grasshoppers application of this paradigm yielded values of the minimum detectable gap widths that are approximately twice as large than the minimum integration times reported here.