R. Matthias Hennig

Time and timing in the acoustic recognition system of crickets

The songs of many insects exhibit precise timing as the result of repetitive and stereotyped subunits on several time scales. As these signals encode the identity of a species, time and timing are important for the recognition system that analyzes these signals. Crickets are a prominent example as their songs are built from sound pulses that are broadcast in a long trill or as a chirped song. This pattern appears to be analyzed on two timescales, short and long. Recent evidence suggests that song recognition in crickets relies on two computations with respect to time; a short linear-nonlinear (LN) model that operates as a filter for pulse rate and a longer integration time window for monitoring song energy over time. Therefore, there is a twofold role for timing. A filter for pulse rate shows differentiating properties for which the specific timing of excitation and inhibition is important. For an integrator, however, the duration of the time window is more important than the precise timing of events. Here, we first review evidence for the role of LN-models and integration time windows for song recognition in crickets. We then parameterize the filter part by Gabor functions and explore the effects of duration, frequency, phase, and offset as these will correspond to differently timed patterns of excitation and inhibition. These filter properties were compared with known preference functions of crickets and katydids. In a comparative approach, the power for song discrimination by LN-models was tested with the songs of over 100 cricket species. It is demonstrated how the acoustic signals of crickets occupy a simple 2-dimensional space for song recognition that arises from timing, described by a Gabor function, and time, the integration window. Finally, we discuss the evolution of recognition systems in insects based on simple sensory computations.

Computational principles underlying the recognition of acoustic signals in insects

Many animals produce pulse-like signals during acoustic communication. These signals exhibit structure on two time scales: they consist of trains of pulses that are often broadcast in packets—so called chirps. Temporal parameters of the pulse and of the chirp are decisive for female preference. Despite these signals being produced by animals from many different taxa (e.g. frogs, grasshoppers, crickets, bushcrickets, flies), a general framework for their evaluation is still lacking. We propose such a framework, based on a simple and physiologically plausible model. The model consists of feature detectors, whose time-varying output is averaged over the signal and then linearly combined to yield the behavioral preference. We fitted this model to large data sets collected in two species of crickets and found that Gabor filters—known from visual and auditory physiology—explain the preference functions in these two species very well. We further explored the properties of Gabor filters and found a systematic relationship between parameters of the filters and the shape of preference functions. Although these Gabor filters were relatively short, they were also able to explain aspects of the preference for signal parameters on the longer time scale due to the integration step in our model. Our framework explains a wide range of phenomena associated with female preference for a widespread class of signals in an intuitive and physiologically plausible fashion. This approach thus constitutes a valuable tool to understand the functioning and evolution of communication systems in many species.

The Origin of Adaptation in the Auditory Pathway of Locusts Is Specific to Cell Type and Function

We investigated the origin of spike frequency adaptation within a layered sensory network: the auditory pathway of locusts. Spike frequency adaptation as observed in an individual neuron may arise because of intrinsic or presynaptic adaptation mechanisms. To separate the contribution of different mechanisms, we recorded from the same cell during acoustic and intracellular current stimulation. We studied three identified neuron types that are representative for each network layer and participate in processing auditory patterns and localizing sound sources. By comparing current and acoustic stimulation, three distinct patterns of the distribution of adaptation mechanisms within the sensory network emerged: (1) balanced influence of both intrinsic and presynaptic adaptation mechanisms in an interneuron that summates over several receptor afferents (TN1), (2) predominantly inhibiting input as the source for spike frequency adaptation in a cell that transmits both pattern representation and directional information (BSN1), (3) primarily intrinsic, spike-triggered adaptation currents within an interneuron coding exclusively for direction (AN2). The time courses of spike frequency adaptation differed significantly between the cells types. Using the adaptation time constants, we were able to predict signal transmission properties for the different cells. We conclude that the adaptation mechanisms differ greatly among interneurons within this sensory pathway and are a function of their role in information processing.

Computational themes of peripheral processing in the auditory pathway of insects

Hearing in insects serves to gain information in the context of mate finding, predator avoidance or host localization. For these goals, the auditory pathways of insects represent the computational substrate for object recognition and localization. Before these higher level computations can be executed in more central parts of the nervous system, the signals need to be preprocessed in the auditory periphery. Here, we review peripheral preprocessing along four computational themes rather than discussing specific physiological mechanisms: (1) control of sensitivity by adaptation, (2) recoding of amplitude modulations of an acoustic signal into a labeled-line code (3) frequency processing and (4) conditioning for binaural processing. Along these lines, we review evidence for canonical computations carried out in the peripheral auditory pathway and show that despite the vast diversity of insect hearing, signal processing is governed by common computational motifs and principles.

Adaptation and Selective Information Transmission in the Cricket Auditory Neuron AN2

Sensory systems adapt their neural code to changes in the sensory environment, often on multiple time scales. Here, we report a new form of adaptation in a first-order auditory interneuron (AN2) of crickets. We characterize the response of the AN2 neuron to amplitude-modulated sound stimuli and find that adaptation shifts the stimulus–response curves toward higher stimulus intensities, with a time constant of 1.5 s for adaptation and recovery. The spike responses were thus reduced for low-intensity sounds. We then address the question whether adaptation leads to an improvement of the signals representation and compare the experimental results with the predictions of two competing hypotheses: infomax, which predicts that information conveyed about the entire signal range should be maximized, and selective coding, which predicts that “foreground” signals should be enhanced while “background” signals should be selectively suppressed. We test how adaptation changes the input–response curve when presenting signals with two or three peaks in their amplitude distributions, for which selective coding and infomax predict conflicting changes. By means of Bayesian data analysis, we quantify the shifts of the measured response curves and also find a slight reduction of their slopes. These decreases in slopes are smaller, and the absolute response thresholds are higher than those predicted by infomax. Most remarkably, and in contrast to the infomax principle, adaptation actually reduces the amount of encoded information when considering the whole range of input signals. The response curve changes are also not consistent with the selective coding hypothesis, because the amount of information conveyed about the loudest part of the signal does not increase as predicted but remains nearly constant. Less information is transmitted about signals with lower intensity.

A neural mechanism for time-window separation resolves ambiguity of adaptive coding.

The senses of animals are confronted with changing environments and different contexts. Neural adaptation is one important tool to adjust sensitivity to varying intensity ranges. For instance, in a quiet night outdoors, our hearing is more sensitive than when we are confronted with the plurality of sounds in a large city during the day. However, adaptation also removes available information on absolute sound levels and may thus cause ambiguity. Experimental data on the trade-off between benefits and loss through adaptation is scarce and very few mechanisms have been proposed to resolve it. We present an example where adaptation is beneficial for one task—namely, the reliable encoding of the pattern of an acoustic signal—but detrimental for another—the localization of the same acoustic stimulus. With a combination of neurophysiological data, modeling, and behavioral tests, we show that adaptation in the periphery of the auditory pathway of grasshoppers enables intensity-invariant coding of amplitude modulations, but at the same time, degrades information available for sound localization. We demonstrate how focusing the response of localization neurons to the onset of relevant signals separates processing of localization and pattern information temporally. In this way, the ambiguity of adaptive coding can be circumvented and both absolute and relative levels can be processed using the same set of peripheral neurons.

Firing-rate resonances in the peripheral auditory system of the cricket, Gryllus bimaculatus

In many communication systems, information is encoded in the temporal pattern of signals. For rhythmic signals that carry information in specific frequency bands, a neuronal system may profit from tuning its inherent filtering properties towards a peak sensitivity in the respective frequency range. The cricket Gryllus bimaculatus evaluates acoustic communication signals of both conspecifics and predators. The song signals of conspecifics exhibit a characteristic pulse pattern that contains only a narrow range of modulation frequencies. We examined individual neurons (AN1, AN2, ON1) in the peripheral auditory system of the cricket for tuning towards specific modulation frequencies by assessing their firing-rate resonance. Acoustic stimuli with a swept-frequency envelope allowed an efficient characterization of the cells’ modulation transfer functions. Some of the examined cells exhibited tuned band-pass properties. Using simple computational models, we demonstrate how different, cell-intrinsic or network-based mechanisms such as subthreshold resonances, spike-triggered adaptation, as well as an interplay of excitation and inhibition can account for the experimentally observed firing-rate resonances. Therefore, basic neuronal mechanisms that share negative feedback as a common theme may contribute to selectivity in the peripheral auditory pathway of crickets that is designed towards mate recognition and predator avoidance.

Critical Song Features for Auditory Pattern Recognition in Crickets

Many different invertebrate and vertebrate species use acoustic communication for pair formation. In the cricket Gryllus bimaculatus, females recognize their species-specific calling song and localize singing males by positive phonotaxis. The song pattern of males has a clear structure consisting of brief and regular pulses that are grouped into repetitive chirps. Information is thus present on a short and a long time scale. Here, we ask which structural features of the song critically determine the phonotactic performance. To this end we employed artificial neural networks to analyze a large body of behavioral data that measured females’ phonotactic behavior under systematic variation of artificially generated song patterns. In a first step we used four non-redundant descriptive temporal features to predict the female response. The model prediction showed a high correlation with the experimental results. We used this behavioral model to explore the integration of the two different time scales. Our result suggested that only an attractive pulse structure in combination with an attractive chirp structure reliably induced phonotactic behavior to signals. In a further step we investigated all feature sets, each one consisting of a different combination of eight proposed temporal features. We identified feature sets of size two, three, and four that achieve highest prediction power by using the pulse period from the short time scale plus additional information from the long time scale.

Multivariate Phenotypic Evolution: Divergent Acoustic Signals and Sexual Selection in Gryllus Field Crickets

Predicting the response to selection is at the core of evolutionary biology. Presently, thorough understanding of the effects of selection on the multivariate phenotype is lacking, in particular for behavioral traits. Here, we compared multivariate acoustic mating signals among seven field cricket species contrasting two selection regimes: (1) species producing songs with long trains of pulses for which preference functions for acoustic energy (chirp duty cycle) are linear and likely exert strong directional selection (‘trillers’); (2) species producing songs consisting of short chirps and for which preference functions for chirp duty cycle are concave and directional selection is likely weak or absent (‘chirpers’). We compared the phenotypic variance–covariance matrix (P) among species and uncovered two main patterns: First, surprisingly, pulse rate and chirp rate were positively correlated in six of seven species thus suggesting phenotypic coupling of timescales. Second, chirp rate and chirp duty cycle also covaried, but the direction of covariation differed between chirpers (positive) and trillers (negative). Multi-population Bayesian methods for matrix comparisons, Krzanowski’s subspace comparison and tensor analysis, revealed significant variation in P unrelated to phylogenetic distance, but strongly contrasting chirpers and trillers. We also found differences in the predicted selection response between chirpers and trillers. We thus report that variation in P is higher between than within selection regimes. Although effects from drift and shared ancestry cannot be fully excluded, these findings highlight a role for sexual selection in shaping patterns of phenotypic covariation that can ultimately affect the evolutionary trajectory of a multivariate mating signal.

How females of chirping and trilling field crickets integrate the ‘what’ and ‘where’ of male acoustic signals during decision making

In crickets acoustic communication serves mate selection. Female crickets have to perceive and integrate male cues relevant for mate choice while confronted with several different signals in an acoustically diverse background. Overall female decisions are based on the attractiveness of the temporal pattern (informative about the ‘what’) and on signal intensity (informative about the ‘where’) of male calling songs. Here, we investigated how the relevant cues for mate choice are integrated during the decision process by females of five different species of chirping and trilling field crickets. Using a behavioral design, female preferences in no-choice and choice situations for male calling songs differing in pulse rate, modulation depth, intensities, chirp/trill arrangements and temporal shifts were examined. Sensory processing underlying decisions in female field crickets is rather similar as combined evidence suggested that incoming song patterns were analyzed separately by bilaterally paired networks for pattern attractiveness and pattern intensity. A downstream gain control mechanism leads to a weighting of the intensity cue by pattern attractiveness. While remarkable differences between species were observed with respect to specific processing steps, closely related species exhibited more similar preferences than did more distantly related species.